Characterization of Distinct Monocyte Subtypes and Immune Features Associated with HIV, Tuberculosis, and Coronary Artery Disease in a Ugandan Cohort Using Mass Cytometry
Article Sidebar
Main Article Content
Abstract
Background: Coronary artery disease (CAD), tuberculosis (TB), and HIV are major global health concerns. Individuals affected by one or more of these conditions often exhibit chronic inflammation and immune dysregulation, with monocytes playing a central role. Monocyte subsets are known to expand in individuals with HIV, TB, or CAD, but the mechanisms by which these cells contribute to inflammation and immune responses remain poorly understood.
Methods: We employed high-dimensional mass cytometry to characterize monocyte heterogeneity in 61 Ugandan adults with varying combinations of HIV, TB, and subclinical or overt CAD. An integrative approach was used, combining manual gating, unsupervised clustering, and machine learning to identify distinct monocyte phenotypes associated with CAD and TB. Monocyte activation markers soluble CD14 (sCD14) and sCD163 were measured in plasma. CAD was diagnosed by coronary computed tomography angiography. TB was determined by a questionnaire and interferon-gamma release assay (IGRA) testing.
Results: Participants’ demographics and clinical characteristics were similar by CAD or HIV/TB status. Median age was 61 years; 37.7% were female. People living with HIV and latent TB or prior active TB had higher sCD14 plasma levels compared with HIV/TB-negative individuals. Individuals with CAD showed reduced surface expression of the scavenger receptor CD163 on non-classical monocytes. Unsupervised clustering further revealed 2 distinct non-classical monocyte subsets associated with disease states: A CD86dim CX3CR1dim CD45RA+ GPR56+ CXCR3+ subset significantly depleted in individuals with CAD, and a CD86+ CX3CR1++ CD45RA++ GPR56- CD38- CXCR3- subset enriched in individuals with latent TB.
Conclusions: These findings underscore the complexity of the monocyte landscape in CAD progression, particularly in regions where HIV and TB are co-endemic. Our study reveals distinct alterations within 2 non-classical monocyte subpopulations associated with CAD and with HIV/TB, offering mechanistic insights that may support the development of precision biomarkers and immune-targeted therapies across these disease contexts.
Downloads
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Pathogens and Immunity abides by Creative Commons BY 4.0:
http://creativecommons.org/licenses/by/4.0/
This license lets others distribute, remix, tweak, and build upon your work for any lawful purpose, even commercially, as long as they credit you for the original creation. This is the most accommodating of licenses offered. Recommended for maximum dissemination and use of licensed materials. The authors maintain copyright of their materal.
*Due to a template error on our pdfs, articles published from May 20, 2016 to June 24, 2022 incorrectly state the copyright is held by Pathogens and Immunity. Copyright of all articles is held by the authors of each article as noted in the above copyright policy.
References
1. Govender RD, Hashim MJ, Khan MA, Mustafa H, Khan G. Global Epidemiology of Hiv/Aids: A Resurgence in North America and Europe. J Epidemiol Glob Health. 2021;11(3):296-301. doi: 10.2991/jegh.k.210621.001. PubMed PMID: 34270183; PMCID: PMC8435868.
2. Berida T, Lindsley CW. Move over Covid, Tuberculosis Is Once Again the Leading Cause of Death from a Single Infectious Disease. J Med Chem. 2024;67(24):21633-40. doi: 10.1021/acs.jmedchem.4c02876. PubMed PMID: 39652566.
3. Gaidai O, Cao Y, Loginov S. Global Cardiovascular Diseases Death Rate Prediction. Curr Probl Cardiol. 2023;48(5):101622. doi: 10.1016/j.cpcardiol.2023.101622. PubMed PMID: 36724816.
4. Siedner MJ, Ghoshhajra B, Erem G, Nassanga R, Randhawa M, Ochieng A, Acan M, Lu MT, Thondapu V, Takigami A, Reynolds Z, Atwiine F, Tindimwebwa E, Gilbert RF, Passell E, Sagar S, Tong Y, Ntusi NAB, Tsai AC, Bibangambah P, Gaziano T, Hoeppner SS, Longenecker CT, Okello S, Asiimwe S. Epidemiology of Coronary Atherosclerosis among People Living with Hiv in Uganda : A Cross-Sectional Study. Ann Intern Med. 2025;178(4):468-78. doi: 10.7326/annals-24-02233. PubMed PMID: 40073231; PMCID: PMC12022967.
5. Hyle EP, Mayosi BM, Middelkoop K, Mosepele M, Martey EB, Walensky RP, Bekker LG, Triant VA. The Association between Hiv and Atherosclerotic Cardiovascular Disease in Sub-Saharan Africa: A Systematic Review. BMC Public Health. 2017;17(1):954. doi: 10.1186/s12889-017-4940-1. PubMed PMID: 29246206; PMCID: PMC5732372.
6. Feria MG, Chang C, Ticona E, Moussa A, Zhang B, Ballena I, Azañero R, Ticona C, De Cecco CN, Fichtenbaum CJ, O’Donnell RE, La Rosa A, Sanchez J, Andorf S, Atehortua L, Katz JD, Chougnet CA, Deepe GS, Jr., Huaman MA. Pro-Inflammatory Alterations of Circulating Monocytes in Latent Tuberculosis Infection. Open Forum Infect Dis. 2022;9(12):ofac629. doi: 10.1093/ofid/ofac629. PubMed PMID: 36570965; PMCID: PMC9772871.
7. Okello S, Amir A, Bloomfield GS, Kentoffio K, Lugobe HM, Reynolds Z, Magodoro IM, North CM, Okello E, Peck R, Siedner MJ. Prevention of Cardiovascular Disease among People Living with Hiv in Sub-Saharan Africa. Prog Cardiovasc Dis. 2020;63(2):149-59. doi: 10.1016/j.pcad.2020.02.004. PubMed PMID: 32035126; PMCID: PMC7237320.
8. Obare LM, Temu T, Mallal SA, Wanjalla CN. Inflammation in Hiv and Its Impact on Atherosclerotic Cardiovascular Disease. Circ Res. 2024;134(11):1515-45. doi: 10.1161/circresaha.124.323891. PubMed PMID: 38781301; PMCID: PMC11122788.
9. Rambaran S, Maseko TG, Lewis L, Hassan-Moosa R, Archary D, Ngcapu S, Garrett N, McKinnon LR, Padayatchi N, Naidoo K, Sivro A. Blood Monocyte and Dendritic Cell Profiles among People Living with Hiv with Mycobacterium Tuberculosis Co-Infection. BMC Immunol. 2023;24(1):21. doi: 10.1186/s12865-023-00558-z. PubMed PMID: 37480005; PMCID: PMC10362598.
10. Huaman MA, Henson D, Ticona E, Sterling TR, Garvy BA. Tuberculosis and Cardiovascular Disease: Linking the Epidemics. Trop Dis Travel Med Vaccines. 2015;1. doi: 10.1186/s40794-015-0014-5. PubMed PMID: 26835156; PMCID: PMC4729377.
11. Chidambaram V, Ruelas Castillo J, Kumar A, Wei J, Wang S, Majella MG, Gupte A, Wang JY, Karakousis PC. The Association of Atherosclerotic Cardiovascular Disease and Statin Use with Inflammation and Treatment Outcomes in Tuberculosis. Sci Rep. 2021;11(1):15283. doi: 10.1038/s41598-021-94590-x. PubMed PMID: 34315941; PMCID: PMC8316554.
12. Knudsen AD, Bouazzi R, Afzal S, Gelpi M, Benfield T, Høgh J, Thomsen MT, Trøseid M, Nordestgaard BG, Nielsen SD. Monocyte Count and Soluble Markers of Monocyte Activation in People Living with Hiv and Uninfected Controls. BMC Infect Dis. 2022;22(1):451. doi: 10.1186/s12879-022-07450-y. PubMed PMID: 35546661; PMCID: PMC9097376.
13. Wallis ZK, Williams KC. Monocytes in Hiv and Siv Infection and Aging: Implications for Inflamm-Aging and Accelerated Aging. Viruses. 2022;14(2). doi: 10.3390/v14020409. PubMed PMID: 35216002; PMCID: PMC8880456.
14. Lyu M, Xu G, Zhou J, Reboud J, Wang Y, Lai H, Chen Y, Zhou Y, Zhu G, Cooper JM, Ying B. Single-Cell Sequencing Reveals Functional Alterations in Tuberculosis. Adv Sci (Weinh). 2024;11(11):e2305592. doi: 10.1002/advs.202305592. PubMed PMID: 38192178; PMCID: PMC10953544.
15. Ji H, Li Y, Fan Z, Zuo B, Jian X, Li L, Liu T. Monocyte/Lymphocyte Ratio Predicts the Severity of Coronary Artery Disease: A Syntax Score Assessment. BMC Cardiovasc Disord. 2017;17(1):90. doi: 10.1186/s12872-017-0507-4. PubMed PMID: 28359298; PMCID: PMC5374608.
16. Moroni F, Ammirati E, Norata GD, Magnoni M, Camici PG. The Role of Monocytes and Macrophages in Human Atherosclerosis, Plaque Neoangiogenesis, and Atherothrombosis. Mediators Inflamm. 2019;2019:7434376. doi: 10.1155/2019/7434376. PubMed PMID: 31089324; PMCID: PMC6476044.
17. Tapp LD, Shantsila E, Wrigley BJ, Pamukcu B, Lip GY. The Cd14++Cd16+ Monocyte Subset and Monocyte-Platelet Interactions in Patients with St-Elevation Myocardial Infarction. J Thromb Haemost. 2012;10(7):1231-41. doi: 10.1111/j.1538-7836.2011.04603.x. PubMed PMID: 22212813.
18. Eligini S, Cosentino N, Fiorelli S, Fabbiocchi F, Niccoli G, Refaat H, Camera M, Calligaris G, De Martini S, Bonomi A, Veglia F, Fracassi F, Crea F, Marenzi G, Tremoli E. Biological Profile of Monocyte-Derived Macrophages in Coronary Heart Disease Patients: Implications for Plaque Morphology. Sci Rep. 2019;9(1):8680. doi: 10.1038/s41598-019-44847-3. PubMed PMID: 31213640; PMCID: PMC6581961.
19. Amengual J, Barrett TJ. Monocytes and Macrophages in Atherogenesis. Curr Opin Lipidol. 2019;30(5):401-8. doi: 10.1097/mol.0000000000000634. PubMed PMID: 31361625; PMCID: PMC7809604.
20. Sampath P, Moideen K, Ranganathan UD, Bethunaickan R. Monocyte Subsets: Phenotypes and Function in Tuberculosis Infection. Front Immunol. 2018;9:1726. doi: 10.3389/fimmu.2018.01726. PubMed PMID: 30105020; PMCID: PMC6077267.
21. Ma R, Yang W, Guo W, Zhang H, Wang Z, Ge Z. Single-Cell Transcriptome Analysis Reveals the Dysregulated Monocyte State Associated with Tuberculosis Progression. BMC Infect Dis. 2025;25(1):210. doi: 10.1186/s12879-025-10612-3. PubMed PMID: 39939918; PMCID: PMC11823163.
22. Bai R, Li Z, Lv S, Wang R, Hua W, Wu H, Dai L. Persistent Inflammation and Non-Aids Comorbidities during Art: Coming of the Age of Monocytes. Front Immunol. 2022;13:820480. doi: 10.3389/fimmu.2022.820480. PubMed PMID: 35479083; PMCID: PMC9035604.
23. Wong ME, Jaworowski A, Hearps AC. The Hiv Reservoir in Monocytes and Macrophages. Front Immunol. 2019;10:1435. doi: 10.3389/fimmu.2019.01435. PubMed PMID: 31297114; PMCID: PMC6607932.
24. Williams DW, Veenstra M, Gaskill PJ, Morgello S, Calderon TM, Berman JW. Monocytes Mediate Hiv Neuropathogenesis: Mechanisms That Contribute to Hiv Associated Neurocognitive Disorders. Curr HIV Res. 2014;12(2):85-96. doi: 10.2174/1570162x12666140526114526. PubMed PMID: 24862333; PMCID: PMC4351961.
25. Ellery PJ, Tippett E, Chiu YL, Paukovics G, Cameron PU, Solomon A, Lewin SR, Gorry PR, Jaworowski A, Greene WC, Sonza S, Crowe SM. The Cd16+ Monocyte Subset Is More Permissive to Infection and Preferentially Harbors Hiv-1 in Vivo. J Immunol. 2007;178(10):6581-9. doi: 10.4049/jimmunol.178.10.6581. PubMed PMID: 17475889.
26. Longenecker CT, Bogorodskaya M, Margevicius S, Nazzinda R, Bittencourt MS, Erem G, Nalukwago S, Huaman MA, Ghoshhajra BB, Siedner MJ, Juchnowski SM, Zidar DA, McComsey GA, Kityo C. Sex Modifies the Association between Hiv and Coronary Artery Disease among Older Adults in Uganda. J Int AIDS Soc. 2022;25(1):e25868. doi: 10.1002/jia2.25868. PubMed PMID: 34995413; PMCID: PMC8741262.
27. Goff DC, Jr., Lloyd-Jones DM, Bennett G, Coady S, D’Agostino RB, Gibbons R, Greenland P, Lackland DT, Levy D, O’Donnell CJ, Robinson JG, Schwartz JS, Shero ST, Smith SC, Jr., Sorlie P, Stone NJ, Wilson PW, Jordan HS, Nevo L, Wnek J, Anderson JL, Halperin JL, Albert NM, Bozkurt B, Brindis RG, Curtis LH, DeMets D, Hochman JS, Kovacs RJ, Ohman EM, Pressler SJ, Sellke FW, Shen WK, Smith SC, Jr., Tomaselli GF. 2013 Acc/Aha Guideline on the Assessment of Cardiovascular Risk: A Report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Circulation. 2014;129(25 Suppl 2):S49-73. doi: 10.1161/01.cir.0000437741.48606.98. PubMed PMID: 24222018.
28. Alencherry B, Erem G, Mirembe G, Ssinabulya I, Yun CH, Hung CL, Siedner MJ, Bittencourt M, Kityo C, McComsey GA, Longenecker CT. Coronary Artery Calcium, Hiv and Inflammation in Uganda Compared with the USA. Open Heart. 2019;6(1):e001046. doi: 10.1136/openhrt-2019-001046. PubMed PMID: 31218009; PMCID: PMC6546194.
29. Min JK, Shaw LJ, Devereux RB, Okin PM, Weinsaft JW, Russo DJ, Lippolis NJ, Berman DS, Callister TQ. Prognostic Value of Multidetector Coronary Computed Tomographic Angiography for Prediction of All-Cause Mortality. J Am Coll Cardiol. 2007;50(12):1161-70. doi: 10.1016/j.jacc.2007.03.067. PubMed PMID: 17868808.
30. Hahne F, LeMeur N, Brinkman RR, Ellis B, Haaland P, Sarkar D, Spidlen J, Strain E, Gentleman R. Flowcore: A Bioconductor Package for High Throughput Flow Cytometry. BMC Bioinformatics. 2009;10:106. doi: 10.1186/1471-2105-10-106. PubMed PMID: 19358741; PMCID: PMC2684747.
31. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: Open Software Development for Computational Biology and Bioinformatics. Genome Biol. 2004;5(10):R80. doi: 10.1186/gb-2004-5-10-r80. PubMed PMID: 15461798; PMCID: PMC545600.
32. Bendall SC, Simonds EF, Qiu P, Amir el AD, Krutzik PO, Finck R, Bruggner RV, Melamed R, Trejo A, Ornatsky OI, Balderas RS, Plevritis SK, Sachs K, Pe’er D, Tanner SD, Nolan GP. Single-Cell Mass Cytometry of Differential Immune and Drug Responses across a Human Hematopoietic Continuum. Science. 2011;332(6030):687-96. doi: 10.1126/science.1198704. PubMed PMID: 21551058; PMCID: PMC3273988.
33. Van Gassen S, Callebaut B, Van Helden MJ, Lambrecht BN, Demeester P, Dhaene T, Saeys Y. Flowsom: Using Self-Organizing Maps for Visualization and Interpretation of Cytometry Data. Cytometry A. 2015;87(7):636-45. doi: 10.1002/cyto.a.22625. PubMed PMID: 25573116.
34. Nowicka M, Krieg C, Crowell HL, Weber LM, Hartmann FJ, Guglietta S, Becher B, Levesque MP, Robinson MD. Cytof Workflow: Differential Discovery in High-Throughput High-Dimensional Cytometry Datasets. F1000Res. 2017;6:748. doi: 10.12688/f1000research.11622.3. PubMed PMID: 28663787; PMCID: PMC5473464.
35. Leland McInnes JH, James Melville. Umap: Uniform Manifold Approximation and Projection for Dimension Reduction [website]. arXiv2020. Available from: https://arxiv.org/abs/1802.03426.
36. Zou H, Hastie T. Regularization and Variable Selection Via the Elastic Net. Journal of the Royal Statistical Society Series B: Statistical Methodology. 2005;67(2):301-20. doi: 10.1111/j.1467-9868.2005.00503.x.
37. William H. Kruskal WAW. Use of Ranks in One-Criterion Variance Analysis [Website]. Journal of the American Statistical Association1952. Available from: https://webspace.ship.edu/pgmarr/Geo441/Readings/Kruskal%20and%20Wallis%201952%20-%20Use%20of%20Ranks%20in%20One-Criterion%20Variance%20Analysis.pdf.
38. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society: Series B (Methodological). 1995;57(1):289-300. doi: https://doi.org/10.1111/j.2517-6161.1995.tb02031.x.
39. Wilcoxon F. Individual Comparisons by Ranking Methods. In: Kotz S, Johnson NL, editors. Breakthroughs in Statistics: Methodology and Distribution. New York, NY: Springer New York; 1992. p. 196-202.
40. Lawn SD, Labeta MO, Arias M, Acheampong JW, Griffin GE. Elevated Serum Concentrations of Soluble Cd14 in Hiv- and Hiv+ Patients with Tuberculosis in Africa: Prolonged Elevation during Anti-Tuberculosis Treatment. Clin Exp Immunol. 2000;120(3):483-7. doi: 10.1046/j.1365-2249.2000.01246.x. PubMed PMID: 10844527; PMCID: PMC1905566.
41. Durda P, Raffield LM, Lange EM, Olson NC, Jenny NS, Cushman M, Deichgraeber P, Grarup N, Jonsson A, Hansen T, Mychaleckyj JC, Psaty BM, Reiner AP, Tracy RP, Lange LA. Circulating Soluble Cd163, Associations with Cardiovascular Outcomes and Mortality, and Identification of Genetic Variants in Older Individuals: The Cardiovascular Health Study. J Am Heart Assoc. 2022;11(21):e024374. doi: 10.1161/jaha.121.024374. PubMed PMID: 36314488; PMCID: PMC9673628.
42. Aristoteli LP, Møller HJ, Bailey B, Moestrup SK, Kritharides L. The Monocytic Lineage Specific Soluble Cd163 Is a Plasma Marker of Coronary Atherosclerosis. Atherosclerosis. 2006;184(2):342-7. doi: 10.1016/j.atherosclerosis.2005.05.004. PubMed PMID: 15979079.
43. Moreno JA, Ortega-Gómez A, Delbosc S, Beaufort N, Sorbets E, Louedec L, Esposito-Farèse M, Tubach F, Nicoletti A, Steg PG, Michel JB, Feldman L, Meilhac O. In Vitro and in Vivo Evidence for the Role of Elastase Shedding of Cd163 in Human Atherothrombosis. Eur Heart J. 2012;33(2):252-63. doi: 10.1093/eurheartj/ehr123. PubMed PMID: 21606088.
44. Etzerodt A, Moestrup SK. Cd163 and Inflammation: Biological, Diagnostic, and Therapeutic Aspects. Antioxid Redox Signal. 2013;18(17):2352-63. doi: 10.1089/ars.2012.4834. PubMed PMID: 22900885; PMCID: PMC3638564.
45. Subauste CS, de Waal Malefyt R, Fuh F. Role of Cd80 (B7.1) and Cd86 (B7.2) in the Immune Response to an Intracellular Pathogen1. The Journal of Immunology. 1998;160(4):1831-40. doi: 10.4049/jimmunol.160.4.1831.
46. Thomas G, Tacke R, Hedrick CC, Hanna RN. Nonclassical Patrolling Monocyte Function in the Vasculature. Arterioscler Thromb Vasc Biol. 2015;35(6):1306-16. doi: 10.1161/atvbaha.114.304650. PubMed PMID: 25838429; PMCID: PMC4441550.
47. Tahir S, Steffens S. Nonclassical Monocytes in Cardiovascular Physiology and Disease. Am J Physiol Cell Physiol. 2021;320(5):C761-c70. doi: 10.1152/ajpcell.00326.2020. PubMed PMID: 33596150.
48. Yona S, Lin HH, Dri P, Davies JQ, Hayhoe RP, Lewis SM, Heinsbroek SE, Brown KA, Perretti M, Hamann J, Treacher DF, Gordon S, Stacey M. Ligation of the Adhesion-Gpcr Emr2 Regulates Human Neutrophil Function. Faseb j. 2008;22(3):741-51. doi: 10.1096/fj.07-9435com. PubMed PMID: 17928360.
49. Altara R, Mallat Z, Booz GW, Zouein FA. The Cxcl10/Cxcr3 Axis and Cardiac Inflammation: Implications for Immunotherapy to Treat Infectious and Noninfectious Diseases of the Heart. J Immunol Res. 2016;2016:4396368. doi: 10.1155/2016/4396368. PubMed PMID: 27795961; PMCID: PMC5066021.
50. Mohapatra A, Howard Z, Ernst JD. Ccr2 Recruits Monocytes to the Lung, While Cx3cr1 Modulates Positioning of Monocyte-Derived Cd11c (Pos) Cells in the Lymph Node during Pulmonary Tuberculosis. bioRxiv. 2025. doi: 10.1101/2025.02.07.637199. PubMed PMID: 39974908; PMCID: PMC11839135.
51. Landsman L, Bar-On L, Zernecke A, Kim KW, Krauthgamer R, Shagdarsuren E, Lira SA, Weissman IL, Weber C, Jung S. Cx3cr1 Is Required for Monocyte Homeostasis and Atherogenesis by Promoting Cell Survival. Blood. 2009;113(4):963-72. doi: 10.1182/blood-2008-07-170787. PubMed PMID: 18971423.
52. Chavakis T, Mitroulis I, Hajishengallis G. Hematopoietic Progenitor Cells as Integrative Hubs for Adaptation to and Fine-Tuning of Inflammation. Nat Immunol. 2019;20(7):802-11. doi: 10.1038/s41590-019-0402-5. PubMed PMID: 31213716; PMCID: PMC6709414.
53. Mildner A, Kim KW, Yona S. Unravelling Monocyte Functions: From the Guardians of Health to the Regulators of Disease. Discov Immunol. 2024;3(1):kyae014. doi: 10.1093/discim/kyae014. PubMed PMID: 39430099; PMCID: PMC11486918.
54. Guo N, Chen Y, Su B, Yang X, Zhang Q, Song T, Wu H, Liu C, Liu L, Zhang T. Alterations of Ccr2 and Cx3cr1 on Three Monocyte Subsets during Hiv-1/Treponema Pallidum Coinfection. Front Med (Lausanne). 2020;7:272. doi: 10.3389/fmed.2020.00272. PubMed PMID: 32626718; PMCID: PMC7314900.
55. Sbrana S, Campolo J, Clemente A, Bastiani L, Cecchettini A, Ceccherini E, Caselli C, Neglia D, Parodi O, Chiappino D, Smit JM, Scholte AJ, Pelosi G, Rocchiccioli S. Blood Monocyte Phenotype Fingerprint of Stable Coronary Artery Disease: A Cross-Sectional Substudy of Smartool Clinical Trial. Biomed Res Int. 2020;2020:8748934. doi: 10.1155/2020/8748934. PubMed PMID: 32802883; PMCID: PMC7403909.
56. Patel VK, Williams H, Li SCH, Fletcher JP, Medbury HJ. Monocyte Inflammatory Profile Is Specific for Individuals and Associated with Altered Blood Lipid Levels. Atherosclerosis. 2017;263:15-23. doi: 10.1016/j.atherosclerosis.2017.05.026. PubMed PMID: 28570862.
57. SahBandar IN, Ndhlovu LC, Saiki K, Kohorn LB, Peterson MM, D’Antoni ML, Shiramizu B, Shikuma CM, Chow DC. Relationship between Circulating Inflammatory Monocytes and Cardiovascular Disease Measures of Carotid Intimal Thickness. J Atheroscler Thromb. 2020;27(5):441-8. doi: 10.5551/jat.49791. PubMed PMID: 31588100; PMCID: PMC7242227.
58. Padgett LE, Araujo DJ, Hedrick CC, Olingy CE. Functional Crosstalk between T Cells and Monocytes in Cancer and Atherosclerosis. J Leukoc Biol. 2020;108(1):297-308. doi: 10.1002/jlb.1mir0420-076r. PubMed PMID: 32531833; PMCID: PMC8006924.
59. Kim KW, Ivanov S, Williams JW. Monocyte Recruitment, Specification, and Function in Atherosclerosis. Cells. 2020;10(1). doi: 10.3390/cells10010015. PubMed PMID: 33374145; PMCID: PMC7823291.
60. Li B, Shaikh F, Zamzam A, Abdin R, Qadura M. Inflammatory Biomarkers to Predict Major Adverse Cardiovascular Events in Patients with Carotid Artery Stenosis. Medicina (Kaunas). 2024;60(6). doi: 10.3390/medicina60060997. PubMed PMID: 38929614; PMCID: PMC11205582.
61. Wiche Salinas TR, Zhang Y, Gosselin A, Rosario NF, El-Far M, Filali-Mouhim A, Routy JP, Chartrand-Lefebvre C, Landay AL, Durand M, Tremblay CL, Ancuta P. Alterations in Th17 Cells and Non-Classical Monocytes as a Signature of Subclinical Coronary Artery Atherosclerosis during Art-Treated Hiv-1 Infection. Cells. 2024;13(2). doi: 10.3390/cells13020157. PubMed PMID: 38247848; PMCID: PMC10813976.