Abstract
Background: Human immunodeficiency virus infection is a recognized risk factor for premature atherosclerosis in children and adolescents. However, the atherosclerotic process in uninfected children exposed in utero to the virus and antiretroviral therapy is less clear.
Objective: To determine the potential cardiovascular risk associated to this in utero milieu exposition. Material and Methods: A total of 115 individuals were studied (77 in the sample group and 38 in the controls). Eighteen analytical mediators involved in the atherogenic pathways (metabolic dysregulation, inflammation, and prothrombotic state) were analyzed. The carotid intima-media thickness, which is a subclinical marker of atherosclerosis, was also measured. Results: No significant statistical differences were identified between the sample and control groups, either in the biochemical or the echographic markers. Conclusion: In utero exposure to the HIV virus and antiretroviral therapy in uninfected children and adolescents is not correlated to accelerated atherosclerosis.Keywords: Antiretroviral therapy, atherosclerosis, carotid intima-media thickness, exposed, child, HIV infection.
[1]
Expert Panel on Integrated Guidelines for Cardiovascular Health and Risk Reduction in Children and Adolescents; National Heart, Lung, and Blood Institute. Expert panel on integrated guidelines for cardiovascular health and risk reduction in children and adolescents: summary report. Pediatrics 2011; 128(Suppl. 5): S213-56.
[http://dx.doi.org/10.1542/peds.2009-2107C] [PMID: 22084329]
[http://dx.doi.org/10.1542/peds.2009-2107C] [PMID: 22084329]
[2]
Kavey RE, Allada V, Daniels SR, et al. American Heart Association Expert Panel on Population and Prevention Science; American Heart Association Council on Cardiovascular Disease in the Young; American Heart Association Council on Epidemiology and Prevention; American Heart Association Council on Nutrition, Physical Activity and Metabolism; American Heart Association Council on High Blood Pressure Research; American Heart Association Council on Cardiovascular Nursing; American Heart Association Council on the Kidney in Heart Disease; Interdisciplinary Working Group on Quality of Care and Outcomes Research. Cardiovascular risk reduction in high-risk pediatric patients: a scientific statement from the American Heart Association Expert Panel on Population and Prevention Science; the Councils on Cardiovascular Disease in the Young, Epidemiology and Prevention, Nutrition, Physical Activity and Metabolism, High Blood Pressure Research, Cardiovascular Nursing, and the Kidney in Heart Disease; and the Interdisciplinary Working Group on Quality of Care and Outcomes Research: endorsed by the American Academy of Pediatrics. Circulation 2006; 114(24): 2710-38.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.106.179568] [PMID: 17130340]
[http://dx.doi.org/10.1161/CIRCULATIONAHA.106.179568] [PMID: 17130340]
[3]
Charakida M, Donald AE, Green H, et al. Early structural and functional changes of the vasculature in HIV-infected children: impact of disease and antiretroviral therapy. Circulation 2005; 112(1): 103-9.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.104.517144] [PMID: 15983247]
[http://dx.doi.org/10.1161/CIRCULATIONAHA.104.517144] [PMID: 15983247]
[4]
McComsey GA, O’Riordan M, Hazen SL, et al. Increased carotid intima media thickness and cardiac biomarkers in HIV infected children. AIDS 2007; 21(8): 921-7.
[http://dx.doi.org/10.1097/QAD.0b013e328133f29c] [PMID: 17457085]
[http://dx.doi.org/10.1097/QAD.0b013e328133f29c] [PMID: 17457085]
[5]
Ross AC, Storer N, O’Riordan MA, Dogra V, McComsey GA. Longitudinal changes in carotid intima-media thickness and cardiovascular risk factors in human immunodeficiency virus-infected children and young adults compared with healthy controls. Pediatr Infect Dis J 2010; 29(7): 634-8.
[http://dx.doi.org/10.1097/INF.0b013e3181d770c4] [PMID: 20589981]
[http://dx.doi.org/10.1097/INF.0b013e3181d770c4] [PMID: 20589981]
[6]
Hanna DB, Guo M, Bůžková P, et al. HIV Infection and Carotid Artery Intima-media Thickness: Pooled Analyses Across 5 Cohorts of the NHLBI HIV-CVD Collaborative. Clin Infect Dis 2016; 63(2): 249-56.
[http://dx.doi.org/10.1093/cid/ciw261] [PMID: 27118787]
[http://dx.doi.org/10.1093/cid/ciw261] [PMID: 27118787]
[7]
Chanthong P, Lapphra K, Saihongthong S, et al. Echocardiography and carotid intima-media thickness among asymptomatic HIV-infected adolescents in Thailand. AIDS 2014; 28(14): 2071-9.
[http://dx.doi.org/10.1097/QAD.0000000000000376] [PMID: 25265075]
[http://dx.doi.org/10.1097/QAD.0000000000000376] [PMID: 25265075]
[8]
Bonnet D, Aggoun Y, Szezepanski I, Bellal N, Blanche S. Arterial stiffness and endothelial dysfunction in HIV-infected children. AIDS 2004; 18(7): 1037-41.
[http://dx.doi.org/10.1097/00002030-200404300-00012] [PMID: 15096807]
[http://dx.doi.org/10.1097/00002030-200404300-00012] [PMID: 15096807]
[9]
Giuliano IdeC, de Freitas SF, de Souza M, Caramelli B. Subclinic atherosclerosis and cardiovascular risk factors in HIV-infected children: PERI study. Coron Artery Dis 2008; 19(3): 167-72.
[http://dx.doi.org/10.1097/MCA.0b013e3282f6dffb] [PMID: 18418233]
[http://dx.doi.org/10.1097/MCA.0b013e3282f6dffb] [PMID: 18418233]
[10]
Augustemak de Lima LR, Petroski EL, Moreno YMF, et al. Dyslipidemia, chronic inflammation, and subclinical atherosclerosis in children and adolescents infected with HIV: The PositHIVe Health Study. PLoS One 2018; 13(1)
[http://dx.doi.org/10.1371/journal.pone.0190785] [PMID: 29320547]
[http://dx.doi.org/10.1371/journal.pone.0190785] [PMID: 29320547]
[11]
Martins P, Castela E, Rocha G, Sena C, Seiça R. Premature Atherosclerosis in HIV-Infected Pediatric Patients: Literature Review and Clinical Approach Acta Med Port 2017; 30(10): 742-9.
[http://dx.doi.org/10.20344/amp.8726] [PMID: 29268069]
[http://dx.doi.org/10.20344/amp.8726] [PMID: 29268069]
[12]
Barlow-Mosha L, Eckard AR, McComsey GA, Musoke PM. Metabolic complications and treatment of perinatally HIV-infected children and adolescents. J Int AIDS Soc 2013; 16: 18600.
[http://dx.doi.org/10.7448/IAS.16.1.18600] [PMID: 23782481]
[http://dx.doi.org/10.7448/IAS.16.1.18600] [PMID: 23782481]
[13]
Prendergast AJ. Complications of long-term antiretroviral therapy in HIV-infected children. Arch Dis Child 2013; 98(4): 245-6.
[http://dx.doi.org/10.1136/archdischild-2012-303215] [PMID: 23413313]
[http://dx.doi.org/10.1136/archdischild-2012-303215] [PMID: 23413313]
[14]
Farley J, Gona P, Crain M, et al. Pediatric AIDS Clinical Trials Group Study 219C Team. Prevalence of elevated cholesterol and associated risk factors among perinatally HIV-infected children (4-19 years old) in Pediatric AIDS Clinical Trials Group 219C. J Acquir Immune Defic Syndr 2005; 38(4): 480-7.
[http://dx.doi.org/10.1097/01.qai.0000139397.30612.96] [PMID: 15764965]
[http://dx.doi.org/10.1097/01.qai.0000139397.30612.96] [PMID: 15764965]
[15]
Tassiopoulos K, Williams PL, Seage GR III, Crain M, Oleske J, Farley J. International Maternal Pediatric Adolescent AIDS Clinical Trials 219C Team. Association of hypercholesterolemia incidence with antiretroviral treatment, including protease inhibitors, among perinatally HIV-infected children. J Acquir Immune Defic Syndr 2008; 47(5): 607-14.
[http://dx.doi.org/10.1097/QAI.0b013e3181648e16] [PMID: 18209684]
[http://dx.doi.org/10.1097/QAI.0b013e3181648e16] [PMID: 18209684]
[16]
Rhoads MP, Lanigan J, Smith CJ, Lyall H. Effect of specific antiretroviral therapy (ART) drugs on lipid changes and the need for lipid management in children with HIV. J Acquir Immune Defic Syndr 2011; 57: 404-12.
[http://dx.doi.org/10.1097/QAI.0b013e31821d33be] [PMID: 21499114]
[http://dx.doi.org/10.1097/QAI.0b013e31821d33be] [PMID: 21499114]
[17]
Viganò A, Brambilla P, Pattarino G, et al. Long-term evaluation of glucose homeostasis in a cohort of HAART-treated HIV-infected children: a longitudinal, observational cohort study. Clin Drug Investig 2009; 29(2): 101-9.
[http://dx.doi.org/10.2165/0044011-200929020-00004] [PMID: 19133705]
[http://dx.doi.org/10.2165/0044011-200929020-00004] [PMID: 19133705]
[18]
Hazra R, Hance LF, Monteiro JP, et al. NISDI Pediatric Study Group 2012. Insulin resistance and glucose and lipid concentrations in a cohort of perinatally HIV-infected Latin American children. Pediatr Infect Dis J 2013; 32(7): 757-9.
[http://dx.doi.org/10.1097/INF.0b013e318286c774] [PMID: 23360832]
[http://dx.doi.org/10.1097/INF.0b013e318286c774] [PMID: 23360832]
[19]
Blázquez D, Ramos-Amador JT, Saínz T, et al. Lipid and glucose alterations in perinatally-acquired HIV-infected adolescents and young adults. BMC Infect Dis 2015; 15: 119.
[http://dx.doi.org/10.1186/s12879-015-0853-8] [PMID: 25880777]
[http://dx.doi.org/10.1186/s12879-015-0853-8] [PMID: 25880777]
[20]
dos Reis LC, de Carvalho Rondó PH, de Sousa Marques HH, de Andrade SB. Dyslipidaemia and insulin resistance in vertically HIV-infected children and adolescents. Trans R Soc Trop Med Hyg 2011; 105(4): 197-203.
[http://dx.doi.org/10.1016/j.trstmh.2011.01.005] [PMID: 21371728]
[http://dx.doi.org/10.1016/j.trstmh.2011.01.005] [PMID: 21371728]
[21]
Werner ML, Pone MV, Fonseca VM, Chaves CR. Lipodystrophy syndrome and cardiovascular risk factors in children and adolescents infected with HIV/AIDS receiving highly active antiretroviral therapy. J Pediatr (Rio J) 2010; 86(1): 27-32.
[http://dx.doi.org/10.2223/JPED.1961] [PMID: 20151093]
[http://dx.doi.org/10.2223/JPED.1961] [PMID: 20151093]
[22]
Papi L, Menezes AC, Rocha H, et al. Prevalence of lipodystrophy and risk factors for dyslipidemia in HIV-infected children in Brazil. Braz J Infect Dis 2014; 18(4): 394-9.
[http://dx.doi.org/10.1016/j.bjid.2013.12.007] [PMID: 24794884]
[http://dx.doi.org/10.1016/j.bjid.2013.12.007] [PMID: 24794884]
[23]
Innes S, Cotton MF, Haubrich R, et al. High prevalence of lipoatrophy in pre-pubertal South African children on antiretroviral therapy: a cross-sectional study. BMC Pediatr 2012; 12: 183.
[http://dx.doi.org/10.1186/1471-2431-12-183] [PMID: 23176441]
[http://dx.doi.org/10.1186/1471-2431-12-183] [PMID: 23176441]
[24]
Piloya T, Bakeera-Kitaka S, Kekitiinwa A, Kamya MR. Lipodystrophy among HIV-infected children and adolescents on highly active antiretroviral therapy in Uganda: a cross sectional study. J Int AIDS Soc 2012; 15(2): 17427.
[http://dx.doi.org/10.7448/IAS.15.2.17427] [PMID: 22814353]
[http://dx.doi.org/10.7448/IAS.15.2.17427] [PMID: 22814353]
[25]
Bwakura-Dangarembizi M, Musiime V, Szubert AJ, et al. ARROW Trial Team. Prevalence of lipodystrophy and metabolic abnormalities in HIV-infected African children after 3 years on first-line antiretroviral therapy. Pediatr Infect Dis J 2015; 34(2): e23-31.
[http://dx.doi.org/10.1097/INF.0000000000000491] [PMID: 25068287]
[http://dx.doi.org/10.1097/INF.0000000000000491] [PMID: 25068287]
[26]
De Luca A, de Gaetano Donati K, Colafigli M, et al. The association of high-sensitivity c-reactive protein and other biomarkers with cardiovascular disease in patients treated for HIV: a nested case-control study. BMC Infect Dis 2013; 13: 414.
[http://dx.doi.org/10.1186/1471-2334-13-414] [PMID: 24004495]
[http://dx.doi.org/10.1186/1471-2334-13-414] [PMID: 24004495]
[27]
Masiá M, Bernal E, Padilla S, et al. The role of C-reactive protein as a marker for cardiovascular risk associated with antiretroviral therapy in HIV-infected patients. Atherosclerosis 2007; 195(1): 167-71.
[http://dx.doi.org/10.1016/j.atherosclerosis.2006.09.013] [PMID: 17049532]
[http://dx.doi.org/10.1016/j.atherosclerosis.2006.09.013] [PMID: 17049532]
[28]
Miller TL, Somarriba G, Orav EJ, et al. Biomarkers of vascular dysfunction in children infected with human immunodeficiency virus-1. J Acquir Immune Defic Syndr 2010; 55(2): 182-8.
[http://dx.doi.org/10.1097/QAI.0b013e3181e222c9] [PMID: 20531209]
[http://dx.doi.org/10.1097/QAI.0b013e3181e222c9] [PMID: 20531209]
[29]
Ross AC, O’Riordan MA, Storer N, Dogra V, McComsey GA. Heightened inflammation is linked to carotid intima-media thickness and endothelial activation in HIV-infected children. Atherosclerosis 2010; 211(2): 492-8.
[http://dx.doi.org/10.1016/j.atherosclerosis.2010.04.008] [PMID: 20471650]
[http://dx.doi.org/10.1016/j.atherosclerosis.2010.04.008] [PMID: 20471650]
[30]
Pontrelli G, Martino AM, Tchidjou HK, et al. HIV is associated with thrombophilia and high D-dimer in children and adolescents. AIDS 2010; 24(8): 1145-51.
[http://dx.doi.org/10.1097/QAD.0b013e328337b9a0] [PMID: 20168205]
[http://dx.doi.org/10.1097/QAD.0b013e328337b9a0] [PMID: 20168205]
[31]
WHO Multicentre Growth Reference Study Group. WHO Child Growth Standards: Length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: Methods and development. Geneva: World Health Organization 2006.
[32]
de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 2007; 85(9): 660-7.
[http://dx.doi.org/10.2471/BLT.07.043497] [PMID: 18026621]
[http://dx.doi.org/10.2471/BLT.07.043497] [PMID: 18026621]
[33]
Lurbe E, Agabiti-Rosei E, Cruickshank JK, et al. 2016 European Society of Hypertension guidelines for the management of high blood pressure in children and adolescents. J Hypertens 2016; 34(10): 1887-920.
[http://dx.doi.org/10.1097/HJH.0000000000001039] [PMID: 27467768]
[http://dx.doi.org/10.1097/HJH.0000000000001039] [PMID: 27467768]
[34]
National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents. The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 2004; 114(2)(Suppl 4th Report): 555-76.
[http://dx.doi.org/10.1542/peds.114.2.S2.555] [PMID: 15286277]
[http://dx.doi.org/10.1542/peds.114.2.S2.555] [PMID: 15286277]
[35]
Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985; 28(7): 412-9.
[http://dx.doi.org/10.1007/BF00280883] [PMID: 3899825]
[http://dx.doi.org/10.1007/BF00280883] [PMID: 3899825]
[36]
López-Jaramillo P, Gómez-Arbeláez D, López-López J, et al. The role of leptin/adiponectin ratio in metabolic syndrome and diabetes. Horm Mol Biol Clin Investig 2014; 18(1): 37-45.
[http://dx.doi.org/10.1515/hmbci-2013-0053] [PMID: 25389999]
[http://dx.doi.org/10.1515/hmbci-2013-0053] [PMID: 25389999]
[37]
Satoh N, Naruse M, Usui T, et al. Leptin-to-adiponectin ratio as a potential atherogenic index in obese type 2 diabetic patients. Diabetes Care 2004; 27(10): 2488-90.
[http://dx.doi.org/10.2337/diacare.27.10.2488] [PMID: 15451921]
[http://dx.doi.org/10.2337/diacare.27.10.2488] [PMID: 15451921]
[38]
Simova I. Intima-media thickness: Appropriate evaluation and proper measurement, described. E-Journal of the ESC Council for Cardiology Practice 2015; 13: 1.
[39]
Stein JH, Korcarz CE, Hurst RT, et al. American Society of Echocardiography Carotid Intima-Media Thickness Task Force; Endorsed by the Society for Vascular Medicine. Use of carotid ultrasound to identify subclinical vascular disease and evaluate cardiovascular disease risk: a consensus statement from the American Society of Echocardiography Carotid Intima-Media Thickness Task Force. J Am Soc Echocardiogr 2008; 21(2): 93-111.
[http://dx.doi.org/10.1016/j.echo.2007.11.011] [PMID: 18261694]
[http://dx.doi.org/10.1016/j.echo.2007.11.011] [PMID: 18261694]
[40]
Dalla Pozza R, Ehringer-Schetitska D, Fritsch P, Jokinen E, Petropoulos A, Oberhoffer R. Association for European Paediatric Cardiology Working Group Cardiovascular Prevention. Intima media thickness measurement in children: A statement from the Association for European Paediatric Cardiology (AEPC) Working Group on Cardiovascular Prevention endorsed by the Association for European Paediatric Cardiology. Atherosclerosis 2015; 238(2): 380-7.
[http://dx.doi.org/10.1016/j.atherosclerosis.2014.12.029] [PMID: 25555270]
[http://dx.doi.org/10.1016/j.atherosclerosis.2014.12.029] [PMID: 25555270]
[41]
Doyon A, Kracht D, Bayazit AK, et al. 4C Study Consortium. Carotid artery intima-media thickness and distensibility in children and adolescents: reference values and role of body dimensions. Hypertension 2013; 62(3): 550-6.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.113.01297] [PMID: 23817494]
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.113.01297] [PMID: 23817494]
[42]
Martins P, Pires A, Albuquerque ME, et al. Myocardial peak systolic velocity-a tool for cardiac screening of HIV-exposed uninfected children. Eur J Pediatr 2020; 179(3): 395-404.
[http://dx.doi.org/10.1007/s00431-019-03477-7] [PMID: 31761972]
[http://dx.doi.org/10.1007/s00431-019-03477-7] [PMID: 31761972]
[43]
Matturri L, Ottaviani G, Corti G, Lavezzi AM. Pathogenesis of early atherosclerotic lesions in infants. Pathol Res Pract 2004; 200(5): 403-10.
[http://dx.doi.org/10.1016/j.prp.2004.03.004] [PMID: 15239349]
[http://dx.doi.org/10.1016/j.prp.2004.03.004] [PMID: 15239349]
[44]
Skilton MR. Intrauterine risk factors for precocious atherosclerosis. Pediatrics 2008; 121(3): 570-4.
[http://dx.doi.org/10.1542/peds.2007-1801] [PMID: 18310207]
[http://dx.doi.org/10.1542/peds.2007-1801] [PMID: 18310207]
[45]
Qanitha A, de Mol BAJM, Burgner DP, et al. Pregnancy-related conditions and premature coronary heart disease in adult offspring. Heart Asia 2017; 9(1): 90-5.
[http://dx.doi.org/10.1136/heartasia-2017-010896] [PMID: 29259659]
[http://dx.doi.org/10.1136/heartasia-2017-010896] [PMID: 29259659]
[46]
Ciccone MM, Scicchitano P, Salerno C, et al. Aorta structural alterations in term neonates: the role of birth and maternal characteristics. BioMed Res Int 2013; 2013 459168
[http://dx.doi.org/10.1155/2013/459168] [PMID: 23984364]
[http://dx.doi.org/10.1155/2013/459168] [PMID: 23984364]
[47]
Palinski W, Napoli C. The fetal origins of atherosclerosis: maternal hypercholesterolemia, and cholesterol-lowering or antioxidant treatment during pregnancy influence in utero programming and postnatal susceptibility to atherogenesis. FASEB J 2002; 16(11): 1348-60.
[http://dx.doi.org/10.1096/fj.02-0226rev] [PMID: 12205026]
[http://dx.doi.org/10.1096/fj.02-0226rev] [PMID: 12205026]
[48]
Palinski W, Yamashita T, Freigang S, Napoli C. Developmental programming: maternal hypercholesterolemia and immunity influence susceptibility to atherosclerosis. Nutr Rev 2007; 65(12 Pt 2): S182-7.
[http://dx.doi.org/10.1301/nr.2007.dec.S182-S187] [PMID: 18240546]
[http://dx.doi.org/10.1301/nr.2007.dec.S182-S187] [PMID: 18240546]
[49]
Alkemade FE, Gittenberger-de Groot AC, Schiel AE, et al. Intrauterine exposure to maternal atherosclerotic risk factors increases the susceptibility to atherosclerosis in adult life. Arterioscler Thromb Vasc Biol 2007; 27(10): 2228-35.
[http://dx.doi.org/10.1161/01.ATV.0000282193.31936.fd] [PMID: 17656671]
[http://dx.doi.org/10.1161/01.ATV.0000282193.31936.fd] [PMID: 17656671]
[50]
Milei J, Ottaviani G, Lavezzi AM, Grana DR, Stella I, Matturri L. Perinatal and infant early atherosclerotic coronary lesions. Can J Cardiol 2008; 24(2): 137-41.
[http://dx.doi.org/10.1016/S0828-282X(08)70570-1] [PMID: 18273488]
[http://dx.doi.org/10.1016/S0828-282X(08)70570-1] [PMID: 18273488]
[51]
Matturri L, Lavezzi AM, Ottaviani G, Rossi L. Intimal preatherosclerotic thickening of the coronary arteries in human fetuses of smoker mothers. J Thromb Haemost 2003; 1(10): 2234-8.
[http://dx.doi.org/10.1046/j.1538-7836.2003.00409.x] [PMID: 14521609]
[http://dx.doi.org/10.1046/j.1538-7836.2003.00409.x] [PMID: 14521609]
[52]
Gunes T, Akin MA, Canoz O, et al. Aortic intima-media thickness in nicotine-exposed rat pups during gestation and lactation period. Eur J Pediatr 2011; 170(10): 1257-62.
[http://dx.doi.org/10.1007/s00431-011-1432-7] [PMID: 21360026]
[http://dx.doi.org/10.1007/s00431-011-1432-7] [PMID: 21360026]
[53]
Mecchia D, Lavezzi AM, Mauri M, Matturri L. Feto-placental atherosclerotic lesions in intrauterine fetal demise: role of parental cigarette smoking. Open Cardiovasc Med J 2009; 3: 51-6.
[http://dx.doi.org/10.2174/1874192400903010051] [PMID: 19572018]
[http://dx.doi.org/10.2174/1874192400903010051] [PMID: 19572018]
[54]
Skilton MR, Evans N, Griffiths KA, Harmer JA, Celermajer DS. Aortic wall thickness in newborns with intrauterine growth restriction. Lancet 2005; 365(9469): 1484-6.
[http://dx.doi.org/10.1016/S0140-6736(05)66419-7] [PMID: 15850633]
[http://dx.doi.org/10.1016/S0140-6736(05)66419-7] [PMID: 15850633]
[55]
Kuo AH, Li C, Huber HF, Clarke GD, Nathanielsz PW. Intrauterine growth restriction results in persistent vascular mismatch in adulthood. J Physiol 2018; 596(23): 5777-90.
[http://dx.doi.org/10.1113/JP275139] [PMID: 29098705]
[http://dx.doi.org/10.1113/JP275139] [PMID: 29098705]
[56]
Cosmi E, Visentin S, Fanelli T, Mautone AJ, Zanardo V. Aortic intima media thickness in fetuses and children with intrauterine growth restriction. Obstet Gynecol 2009; 114(5): 1109-14.
[http://dx.doi.org/10.1097/AOG.0b013e3181bb23d3] [PMID: 20168114]
[http://dx.doi.org/10.1097/AOG.0b013e3181bb23d3] [PMID: 20168114]
[57]
Visentin S, Londero AP, Calanducci M, et al. Fetal Abdominal Aorta: Doppler and Structural Evaluation of Endothelial Function in Intrauterine Growth Restriction and Controls. Ultraschall Med 2019; 40(1): 55-63.
[http://dx.doi.org/10.1055/s-0043-122230] [PMID: 30253430]
[http://dx.doi.org/10.1055/s-0043-122230] [PMID: 30253430]
[58]
Zanardo V, Fanelli T, Weiner G, et al. Intrauterine growth restriction is associated with persistent aortic wall thickening and glomerular proteinuria during infancy. Kidney Int 2011; 80(1): 119-23.
[http://dx.doi.org/10.1038/ki.2011.99] [PMID: 21490588]
[http://dx.doi.org/10.1038/ki.2011.99] [PMID: 21490588]
[59]
Palinski W, D’Armiento FP, Witztum JL, et al. Maternal hypercholesterolemia and treatment during pregnancy influence the long-term progression of atherosclerosis in offspring of rabbits. Circ Res 2001; 89(11): 991-6.
[http://dx.doi.org/10.1161/hh2301.099646] [PMID: 11717155]
[http://dx.doi.org/10.1161/hh2301.099646] [PMID: 11717155]
[60]
Napoli C, Witztum JL, Calara F, de Nigris F, Palinski W. Maternal hypercholesterolemia enhances atherogenesis in normocholesterolemic rabbits, which is inhibited by antioxidant or lipid-lowering intervention during pregnancy: an experimental model of atherogenic mechanisms in human fetuses. Circ Res 2000; 87(10): 946-52.
[http://dx.doi.org/10.1161/01.RES.87.10.946] [PMID: 11073892]
[http://dx.doi.org/10.1161/01.RES.87.10.946] [PMID: 11073892]
[61]
Napoli C, D’Armiento FP, Mancini FP, et al. Fatty streak formation occurs in human fetal aortas and is greatly enhanced by maternal hypercholesterolemia. Intimal accumulation of low density lipoprotein and its oxidation precede monocyte recruitment into early atherosclerotic lesions. J Clin Invest 1997; 100(11): 2680-90.
[http://dx.doi.org/10.1172/JCI119813] [PMID: 9389731]
[http://dx.doi.org/10.1172/JCI119813] [PMID: 9389731]
[62]
Napoli C, Glass CK, Witztum JL, Deutsch R, D’Armiento FP, Palinski W. Influence of maternal hypercholesterolaemia during pregnancy on progression of early atherosclerotic lesions in childhood: Fate of Early Lesions in Children (FELIC) study. Lancet 1999; 354(9186): 1234-41.
[http://dx.doi.org/10.1016/S0140-6736(99)02131-5] [PMID: 10520631]
[http://dx.doi.org/10.1016/S0140-6736(99)02131-5] [PMID: 10520631]
[63]
Dib A, Payen C, Bourreau J, et al. In Utero Exposure to Maternal Diabetes Is Associated With Early Abnormal Vascular Structure in Offspring. Front Physiol 2018; 9: 350.
[http://dx.doi.org/10.3389/fphys.2018.00350] [PMID: 29670546]
[http://dx.doi.org/10.3389/fphys.2018.00350] [PMID: 29670546]
[64]
Vessières E, Dib A, Bourreau J, et al. Long Lasting Microvascular Tone Alteration in Rat Offspring Exposed In Utero to Maternal Hyperglycaemia. PLoS One 2016; 11(1) e0146830
[http://dx.doi.org/10.1371/journal.pone.0146830] [PMID: 26756337]
[http://dx.doi.org/10.1371/journal.pone.0146830] [PMID: 26756337]
[65]
Duong Van Huyen JP, Vessières E, Perret C, et al. In utero exposure to maternal diabetes impairs vascular expression of prostacyclin receptor in rat offspring. Diabetes 2010; 59(10): 2597-602.
[http://dx.doi.org/10.2337/db10-0311] [PMID: 20622163]
[http://dx.doi.org/10.2337/db10-0311] [PMID: 20622163]
[66]
Bekkering S, Limawan AP, Nguyen MU, et al. Postnatal inflammation following intrauterine inflammation exacerbates the development of atherosclerosis in ApoE-/- mice. Clin Sci (Lond) 2019; 133(10): 1185-96.
[http://dx.doi.org/10.1042/CS20190141] [PMID: 31088858]
[http://dx.doi.org/10.1042/CS20190141] [PMID: 31088858]
[67]
Nguyen MU, Wallace MJ, Pepe S, Menheniott TR, Moss TJ, Burgner D. Perinatal inflammation: a common factor in the early origins of cardiovascular disease? Clin Sci (Lond) 2015; 129(8): 769-84.
[http://dx.doi.org/10.1042/CS20150045] [PMID: 26223841]
[http://dx.doi.org/10.1042/CS20150045] [PMID: 26223841]
[68]
Leduc L, Levy E, Bouity-Voubou M, Delvin E. Fetal programming of atherosclerosis: possible role of the mitochondria. Eur J Obstet Gynecol Reprod Biol 2010; 149(2): 127-30.
[http://dx.doi.org/10.1016/j.ejogrb.2009.12.005] [PMID: 20053495]
[http://dx.doi.org/10.1016/j.ejogrb.2009.12.005] [PMID: 20053495]
[69]
Singer M. A dose of drugs, a touch of violence, a case of AIDS: Conceptualizing the SAVA syndemic. Free Inq Creat Sociol 1996; 24: 99-110.
[70]
Russell BS, Eaton LA, Petersen-Williams P. Intersecting epidemics among pregnant women: alcohol use, interpersonal violence, and HIV infection in South Africa. Curr HIV/AIDS Rep 2013; 10(1): 103-10.
[http://dx.doi.org/10.1007/s11904-012-0145-5] [PMID: 23233038]
[http://dx.doi.org/10.1007/s11904-012-0145-5] [PMID: 23233038]
[71]
Illangasekare S, Burke J, Chander G, Gielen A. The syndemic effects of intimate partner violence, HIV/AIDS, and substance abuse on depression among low-income urban women. J Urban Health 2013; 90(5): 934-47.
[http://dx.doi.org/10.1007/s11524-013-9797-8] [PMID: 23529665]
[http://dx.doi.org/10.1007/s11524-013-9797-8] [PMID: 23529665]
[72]
Miller TI, Borkowsky W, DiMeglio LA, et al. Pediatric HIV/AIDS Cohort Study (PHACS). Metabolic abnormalities and viral replication are associated with biomarkers of vascular dysfunction in HIV-infected children. HIV Med 2012; 13(5): 264-75.
[http://dx.doi.org/10.1111/j.1468-1293.2011.00970.x] [PMID: 22136114]
[http://dx.doi.org/10.1111/j.1468-1293.2011.00970.x] [PMID: 22136114]
[73]
Lipshultz SE, Sasaki N, Thompson B, et al. Left ventricular diastolic dysfunction in HIV-uninfected infants exposed in utero to antiretroviral therapy. AIDS 2020; 34(4): 529-37.
[http://dx.doi.org/10.1097/QAD.0000000000002443] [PMID: 31764073]
[http://dx.doi.org/10.1097/QAD.0000000000002443] [PMID: 31764073]
[74]
Stary HC. Lipid and macrophage accumulations in arteries of children and the development of atherosclerosis. Am J Clin Nutr 2000; 72(5)(Suppl.): 1297S-306S.
[http://dx.doi.org/10.1093/ajcn/72.5.1297s] [PMID: 11063472]
[http://dx.doi.org/10.1093/ajcn/72.5.1297s] [PMID: 11063472]
[75]
Dover GJ. The Barker hypothesis: how pediatricans will diagnose and prevent common adult-onset diseases. Trans Am Clin Climatol Assoc 2009; 120: 199-207.
[PMID: 19768178]
[PMID: 19768178]
[76]
de Boo HA, Harding JE. The developmental origins of adult disease (Barker) hypothesis. Aust N Z J Obstet Gynaecol 2006; 46(1): 4-14.
[http://dx.doi.org/10.1111/j.1479-828X.2006.00506.x] [PMID: 16441686]
[http://dx.doi.org/10.1111/j.1479-828X.2006.00506.x] [PMID: 16441686]
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