Association of Lipidomic Profiles with Progression of Carotid Artery Atherosclerosis in HIV Infection

Jin Choul Chai, Amy A. Deik, Simin Hua, Tao Wang, David B. Hanna, Xiaonan Xue, Sabina A. Haberlen, Sanjiv J. Shah, Yousin Suh, Jason M. Lazar, Deborah Gustafson, Howard N. Hodis, Alan L. Landay, Kathryn Anastos, Wendy S. Post, Robert C. Kaplan, Clary B. Clish, Qibin Qi

Research output: Contribution to journalArticle

Abstract

Importance: Lipid metabolism disruption and excess risk of cardiovascular disease (CVD) have been observed in HIV-infected individuals, but the associations among HIV infection, plasma lipidome, and CVD risk have not been well understood. Objective: To evaluate plasma lipidomic profiles and their associations with carotid artery atherosclerosis in individuals with HIV and individuals without HIV. Design, Setting, and Participants: Prospective analysis in the Women's Interagency HIV Study and Multicenter AIDS Cohort Study during a 7-year follow-up (from 2004-2006 to 2011-2013) at multicenter HIV cohorts in the United States. The study included 737 participants aged 35 to 55 years (520 with HIV and 217 without HIV) without CVD or carotid artery plaque at baseline. Data were analyzed between April 2017 and July 2019. Exposures: Two hundred eleven plasma lipid species. Main Outcomes and Measures: Poisson regression was used to examine the associations of baseline lipid species with risk of plaque measured by repeated B-mode carotid artery ultrasonography imaging. Results: Of the 737 included participants, 398 (54%) were women, 351 (48%) were African American (non-Hispanic), 156 of 737 (21%) were nonwhite Hispanic, and the mean (SD) age was 45 (6) years. After adjusting for demographic and behavioral factors, we identified 12 lipid species, representing independent signals for 10 lipid classes, associated with risk of plaque. Nine lipid species remained significant after further adjusting for conventional CVD risk factors, although many of them showed moderate to high association with conventional blood lipids (eg, total and low-density lipoprotein cholesterols and triglycerides). Cholesteryl ester (16:1) (risk ratio [RR] per standard deviation, 1.28; 95% CI, 1.08-1.52), ceramide (16:0) (RR, 1.29; 95% CI, 1.02-1.63), lysophosphatidylcholine (20:4) (RR, 1.28; 95% CI, 1.05-1.58), lysophosphatidylethanolamine (16:0) (RR, 1.28; 95% CI, 1.05-1.57), phosphatidylethanolamine (38:6) (RR, 1.33; 95% CI, 1.08-1.64), phosphatidylethanolamine-plasmalogen (36:2) (RR, 1.25; 95% CI, 1.04-1.52), phosphatidylserine-plasmalogen (36:3) (RR, 1.19; 95% CI, 1.00-1.43), and triacylglycerol (54:6) (RR, 1.26; 95% CI, 1.04-1.54) were associated with increased risk of plaque, while phosphatidylcholine (36:4) (RR, 0.65; 95% CI, 0.54-0.77) was associated with decreased risk of plaque. Most of these plaque-increased lipid species showed higher levels in individuals with HIV, particularly among individuals with HIV using antiretroviral therapy compared with individuals without HIV. Network analysis identified 9 lipid modules, and 2 modules composed of triacylglycerols and phosphatidylcholines with long and unsaturated acyl chains, respectively, showed the strongest associations with increased risk of plaque. Conclusions and Relevance: This study identified multiple plasma lipid species associated with carotid artery atherosclerosis, and alterations in these lipid species might be associated with HIV infection and antiretroviral therapy. Our data suggest unfavorable associations of long-chain and unsaturated triacylglycerols and phosphatidylcholines with carotid artery plaque formation..

Original languageEnglish (US)
Pages (from-to)1239-1249
Number of pages11
JournalJAMA cardiology
Volume4
Issue number12
DOIs
StatePublished - Dec 2019

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Carotid Artery Diseases
Carotid Arteries
HIV Infections
HIV
Odds Ratio
Lipids
Cardiovascular Diseases
Phosphatidylcholines
Triglycerides
Carotid Stenosis
Plasmalogens
Lysophosphatidylcholines
Cholesterol Esters
Ceramides
Phosphatidylserines
Lipid Metabolism
Hispanic Americans
African Americans
LDL Cholesterol
Multicenter Studies

ASJC Scopus subject areas

  • Cardiology and Cardiovascular Medicine

Cite this

Chai, J. C., Deik, A. A., Hua, S., Wang, T., Hanna, D. B., Xue, X., ... Qi, Q. (2019). Association of Lipidomic Profiles with Progression of Carotid Artery Atherosclerosis in HIV Infection. JAMA cardiology, 4(12), 1239-1249. https://doi.org/10.1001/jamacardio.2019.4025

Association of Lipidomic Profiles with Progression of Carotid Artery Atherosclerosis in HIV Infection. / Chai, Jin Choul; Deik, Amy A.; Hua, Simin; Wang, Tao; Hanna, David B.; Xue, Xiaonan; Haberlen, Sabina A.; Shah, Sanjiv J.; Suh, Yousin; Lazar, Jason M.; Gustafson, Deborah; Hodis, Howard N.; Landay, Alan L.; Anastos, Kathryn; Post, Wendy S.; Kaplan, Robert C.; Clish, Clary B.; Qi, Qibin.

In: JAMA cardiology, Vol. 4, No. 12, 12.2019, p. 1239-1249.

Research output: Contribution to journalArticle

Chai, JC, Deik, AA, Hua, S, Wang, T, Hanna, DB, Xue, X, Haberlen, SA, Shah, SJ, Suh, Y, Lazar, JM, Gustafson, D, Hodis, HN, Landay, AL, Anastos, K, Post, WS, Kaplan, RC, Clish, CB & Qi, Q 2019, 'Association of Lipidomic Profiles with Progression of Carotid Artery Atherosclerosis in HIV Infection', JAMA cardiology, vol. 4, no. 12, pp. 1239-1249. https://doi.org/10.1001/jamacardio.2019.4025
Chai, Jin Choul ; Deik, Amy A. ; Hua, Simin ; Wang, Tao ; Hanna, David B. ; Xue, Xiaonan ; Haberlen, Sabina A. ; Shah, Sanjiv J. ; Suh, Yousin ; Lazar, Jason M. ; Gustafson, Deborah ; Hodis, Howard N. ; Landay, Alan L. ; Anastos, Kathryn ; Post, Wendy S. ; Kaplan, Robert C. ; Clish, Clary B. ; Qi, Qibin. / Association of Lipidomic Profiles with Progression of Carotid Artery Atherosclerosis in HIV Infection. In: JAMA cardiology. 2019 ; Vol. 4, No. 12. pp. 1239-1249.
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title = "Association of Lipidomic Profiles with Progression of Carotid Artery Atherosclerosis in HIV Infection",
abstract = "Importance: Lipid metabolism disruption and excess risk of cardiovascular disease (CVD) have been observed in HIV-infected individuals, but the associations among HIV infection, plasma lipidome, and CVD risk have not been well understood. Objective: To evaluate plasma lipidomic profiles and their associations with carotid artery atherosclerosis in individuals with HIV and individuals without HIV. Design, Setting, and Participants: Prospective analysis in the Women's Interagency HIV Study and Multicenter AIDS Cohort Study during a 7-year follow-up (from 2004-2006 to 2011-2013) at multicenter HIV cohorts in the United States. The study included 737 participants aged 35 to 55 years (520 with HIV and 217 without HIV) without CVD or carotid artery plaque at baseline. Data were analyzed between April 2017 and July 2019. Exposures: Two hundred eleven plasma lipid species. Main Outcomes and Measures: Poisson regression was used to examine the associations of baseline lipid species with risk of plaque measured by repeated B-mode carotid artery ultrasonography imaging. Results: Of the 737 included participants, 398 (54{\%}) were women, 351 (48{\%}) were African American (non-Hispanic), 156 of 737 (21{\%}) were nonwhite Hispanic, and the mean (SD) age was 45 (6) years. After adjusting for demographic and behavioral factors, we identified 12 lipid species, representing independent signals for 10 lipid classes, associated with risk of plaque. Nine lipid species remained significant after further adjusting for conventional CVD risk factors, although many of them showed moderate to high association with conventional blood lipids (eg, total and low-density lipoprotein cholesterols and triglycerides). Cholesteryl ester (16:1) (risk ratio [RR] per standard deviation, 1.28; 95{\%} CI, 1.08-1.52), ceramide (16:0) (RR, 1.29; 95{\%} CI, 1.02-1.63), lysophosphatidylcholine (20:4) (RR, 1.28; 95{\%} CI, 1.05-1.58), lysophosphatidylethanolamine (16:0) (RR, 1.28; 95{\%} CI, 1.05-1.57), phosphatidylethanolamine (38:6) (RR, 1.33; 95{\%} CI, 1.08-1.64), phosphatidylethanolamine-plasmalogen (36:2) (RR, 1.25; 95{\%} CI, 1.04-1.52), phosphatidylserine-plasmalogen (36:3) (RR, 1.19; 95{\%} CI, 1.00-1.43), and triacylglycerol (54:6) (RR, 1.26; 95{\%} CI, 1.04-1.54) were associated with increased risk of plaque, while phosphatidylcholine (36:4) (RR, 0.65; 95{\%} CI, 0.54-0.77) was associated with decreased risk of plaque. Most of these plaque-increased lipid species showed higher levels in individuals with HIV, particularly among individuals with HIV using antiretroviral therapy compared with individuals without HIV. Network analysis identified 9 lipid modules, and 2 modules composed of triacylglycerols and phosphatidylcholines with long and unsaturated acyl chains, respectively, showed the strongest associations with increased risk of plaque. Conclusions and Relevance: This study identified multiple plasma lipid species associated with carotid artery atherosclerosis, and alterations in these lipid species might be associated with HIV infection and antiretroviral therapy. Our data suggest unfavorable associations of long-chain and unsaturated triacylglycerols and phosphatidylcholines with carotid artery plaque formation..",
author = "Chai, {Jin Choul} and Deik, {Amy A.} and Simin Hua and Tao Wang and Hanna, {David B.} and Xiaonan Xue and Haberlen, {Sabina A.} and Shah, {Sanjiv J.} and Yousin Suh and Lazar, {Jason M.} and Deborah Gustafson and Hodis, {Howard N.} and Landay, {Alan L.} and Kathryn Anastos and Post, {Wendy S.} and Kaplan, {Robert C.} and Clish, {Clary B.} and Qibin Qi",
year = "2019",
month = "12",
doi = "10.1001/jamacardio.2019.4025",
language = "English (US)",
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pages = "1239--1249",
journal = "JAMA Cardiology",
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TY - JOUR

T1 - Association of Lipidomic Profiles with Progression of Carotid Artery Atherosclerosis in HIV Infection

AU - Chai, Jin Choul

AU - Deik, Amy A.

AU - Hua, Simin

AU - Wang, Tao

AU - Hanna, David B.

AU - Xue, Xiaonan

AU - Haberlen, Sabina A.

AU - Shah, Sanjiv J.

AU - Suh, Yousin

AU - Lazar, Jason M.

AU - Gustafson, Deborah

AU - Hodis, Howard N.

AU - Landay, Alan L.

AU - Anastos, Kathryn

AU - Post, Wendy S.

AU - Kaplan, Robert C.

AU - Clish, Clary B.

AU - Qi, Qibin

PY - 2019/12

Y1 - 2019/12

N2 - Importance: Lipid metabolism disruption and excess risk of cardiovascular disease (CVD) have been observed in HIV-infected individuals, but the associations among HIV infection, plasma lipidome, and CVD risk have not been well understood. Objective: To evaluate plasma lipidomic profiles and their associations with carotid artery atherosclerosis in individuals with HIV and individuals without HIV. Design, Setting, and Participants: Prospective analysis in the Women's Interagency HIV Study and Multicenter AIDS Cohort Study during a 7-year follow-up (from 2004-2006 to 2011-2013) at multicenter HIV cohorts in the United States. The study included 737 participants aged 35 to 55 years (520 with HIV and 217 without HIV) without CVD or carotid artery plaque at baseline. Data were analyzed between April 2017 and July 2019. Exposures: Two hundred eleven plasma lipid species. Main Outcomes and Measures: Poisson regression was used to examine the associations of baseline lipid species with risk of plaque measured by repeated B-mode carotid artery ultrasonography imaging. Results: Of the 737 included participants, 398 (54%) were women, 351 (48%) were African American (non-Hispanic), 156 of 737 (21%) were nonwhite Hispanic, and the mean (SD) age was 45 (6) years. After adjusting for demographic and behavioral factors, we identified 12 lipid species, representing independent signals for 10 lipid classes, associated with risk of plaque. Nine lipid species remained significant after further adjusting for conventional CVD risk factors, although many of them showed moderate to high association with conventional blood lipids (eg, total and low-density lipoprotein cholesterols and triglycerides). Cholesteryl ester (16:1) (risk ratio [RR] per standard deviation, 1.28; 95% CI, 1.08-1.52), ceramide (16:0) (RR, 1.29; 95% CI, 1.02-1.63), lysophosphatidylcholine (20:4) (RR, 1.28; 95% CI, 1.05-1.58), lysophosphatidylethanolamine (16:0) (RR, 1.28; 95% CI, 1.05-1.57), phosphatidylethanolamine (38:6) (RR, 1.33; 95% CI, 1.08-1.64), phosphatidylethanolamine-plasmalogen (36:2) (RR, 1.25; 95% CI, 1.04-1.52), phosphatidylserine-plasmalogen (36:3) (RR, 1.19; 95% CI, 1.00-1.43), and triacylglycerol (54:6) (RR, 1.26; 95% CI, 1.04-1.54) were associated with increased risk of plaque, while phosphatidylcholine (36:4) (RR, 0.65; 95% CI, 0.54-0.77) was associated with decreased risk of plaque. Most of these plaque-increased lipid species showed higher levels in individuals with HIV, particularly among individuals with HIV using antiretroviral therapy compared with individuals without HIV. Network analysis identified 9 lipid modules, and 2 modules composed of triacylglycerols and phosphatidylcholines with long and unsaturated acyl chains, respectively, showed the strongest associations with increased risk of plaque. Conclusions and Relevance: This study identified multiple plasma lipid species associated with carotid artery atherosclerosis, and alterations in these lipid species might be associated with HIV infection and antiretroviral therapy. Our data suggest unfavorable associations of long-chain and unsaturated triacylglycerols and phosphatidylcholines with carotid artery plaque formation..

AB - Importance: Lipid metabolism disruption and excess risk of cardiovascular disease (CVD) have been observed in HIV-infected individuals, but the associations among HIV infection, plasma lipidome, and CVD risk have not been well understood. Objective: To evaluate plasma lipidomic profiles and their associations with carotid artery atherosclerosis in individuals with HIV and individuals without HIV. Design, Setting, and Participants: Prospective analysis in the Women's Interagency HIV Study and Multicenter AIDS Cohort Study during a 7-year follow-up (from 2004-2006 to 2011-2013) at multicenter HIV cohorts in the United States. The study included 737 participants aged 35 to 55 years (520 with HIV and 217 without HIV) without CVD or carotid artery plaque at baseline. Data were analyzed between April 2017 and July 2019. Exposures: Two hundred eleven plasma lipid species. Main Outcomes and Measures: Poisson regression was used to examine the associations of baseline lipid species with risk of plaque measured by repeated B-mode carotid artery ultrasonography imaging. Results: Of the 737 included participants, 398 (54%) were women, 351 (48%) were African American (non-Hispanic), 156 of 737 (21%) were nonwhite Hispanic, and the mean (SD) age was 45 (6) years. After adjusting for demographic and behavioral factors, we identified 12 lipid species, representing independent signals for 10 lipid classes, associated with risk of plaque. Nine lipid species remained significant after further adjusting for conventional CVD risk factors, although many of them showed moderate to high association with conventional blood lipids (eg, total and low-density lipoprotein cholesterols and triglycerides). Cholesteryl ester (16:1) (risk ratio [RR] per standard deviation, 1.28; 95% CI, 1.08-1.52), ceramide (16:0) (RR, 1.29; 95% CI, 1.02-1.63), lysophosphatidylcholine (20:4) (RR, 1.28; 95% CI, 1.05-1.58), lysophosphatidylethanolamine (16:0) (RR, 1.28; 95% CI, 1.05-1.57), phosphatidylethanolamine (38:6) (RR, 1.33; 95% CI, 1.08-1.64), phosphatidylethanolamine-plasmalogen (36:2) (RR, 1.25; 95% CI, 1.04-1.52), phosphatidylserine-plasmalogen (36:3) (RR, 1.19; 95% CI, 1.00-1.43), and triacylglycerol (54:6) (RR, 1.26; 95% CI, 1.04-1.54) were associated with increased risk of plaque, while phosphatidylcholine (36:4) (RR, 0.65; 95% CI, 0.54-0.77) was associated with decreased risk of plaque. Most of these plaque-increased lipid species showed higher levels in individuals with HIV, particularly among individuals with HIV using antiretroviral therapy compared with individuals without HIV. Network analysis identified 9 lipid modules, and 2 modules composed of triacylglycerols and phosphatidylcholines with long and unsaturated acyl chains, respectively, showed the strongest associations with increased risk of plaque. Conclusions and Relevance: This study identified multiple plasma lipid species associated with carotid artery atherosclerosis, and alterations in these lipid species might be associated with HIV infection and antiretroviral therapy. Our data suggest unfavorable associations of long-chain and unsaturated triacylglycerols and phosphatidylcholines with carotid artery plaque formation..

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