Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Increased carotid artery wall stiffness and plaque prevalence in HIV infected patients measured with ultrasound elastography

  • 13 Accesses

Abstract

Objectives

Assess carotid artery strain and motion in people living with HIV as markers of premature aging using ultrasound noninvasive vascular elastography (NIVE).

Methods

Seventy-four HIV-infected and 75 age-matched control subjects were recruited from a prospective, controlled cohort study from October 2015 to October 2017 (mean age 56 years ± 8 years; 128 men). NIVE applied to longitudinal ultrasound images of common and internal carotid arteries quantified the cumulated axial strain, cumulated shear strain, cumulated axial translation, and cumulated lateral translations. The presence of plaque was also assessed. An association between elastography biomarkers and HIV status was evaluated with Mann–Whitney tests and multivariable linear regression models.

Results

A higher occurrence of carotid artery plaques was found in HIV-infected individuals (p = 0.011). Lower cumulated lateral translations were found in HIV-infected subjects on both common and internal carotid arteries (p = 0.037 and p = 0.026, respectively). These observations remained significant when considering multivariable models including common cardiovascular risk factors and clinical characteristics (p < 0.05). Lower cumulated axial strains were also observed in internal carotid arteries when considering both multivariable models (p < 0.05).

Conclusion

Lower translation and strain of the carotid artery wall in HIV-infected individuals indicates increased vessel wall stiffness. These new imaging biomarkers could be used to characterize premature atherosclerosis development.

Key Points

Noninvasive vascular elastography (NIVE) based on ultrasound imaging quantifies translations and strains of carotid arteries.

Lower translation and strain of the carotid artery wall found in HIV-infected individuals indicate premature arterial stiffening, compared with age-matched controls.

Carotid artery plaques were more prevalent in HIV-infected individuals than in control subjects.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2

Abbreviations

ART:

Antiretroviral therapy

CAS:

Cumulated axial strain

CAT:

Cumulated axial translation

CCA:

Common carotid artery

CHACS:

Canadian HIV and Aging Cohort Study

CLT:

Cumulated lateral translation

C|ShS|:

Cumulated axial shear magnitude

HDL-C:

High-density lipoprotein cholesterol

ICA:

Internal carotid artery

IMT:

Intima-media thickness

LDL-C:

Low-density lipoprotein cholesterol

NIVE:

Noninvasive vascular elastography

References

  1. 1.

    May MT, Gompels M, Delpech V et al (2014) Impact on life expectancy of HIV-1 positive individuals of CD4+ cell count and viral load response to antiretroviral therapy. AIDS 28:1193–1202

  2. 2.

    van Sighem AI, Gras LA, Reiss P, Brinkman K, de Wolf F (2010) Life expectancy of recently diagnosed asymptomatic HIV-infected patients approaches that of uninfected individuals. AIDS 24:1527–1535

  3. 3.

    Antiretroviral Therapy Cohort Collaboration (2008) Life expectancy of individuals on combination antiretroviral therapy in highincome countries: a collaborative analysis of 14 cohort studies. Lancet 372:293–299

  4. 4.

    Deeks SG (2009) Immune dysfunction, inflammation, and accelerated aging in patients on antiretroviral therapy. Top HIV Med 17:118–123

  5. 5.

    Guaraldi G, Orlando G, Zona S et al (2011) Premature age-related comorbidities among HIV-infected persons compared with the general population. Clin Infect Dis 53:1120–1126

  6. 6.

    Gianesin K, Noguera-Julian A, Zanchetta M et al (2016) Premature aging and immune senescence in HIV-infected children. AIDS 30:1363–1373

  7. 7.

    Deeks SG, Phillips AN (2009) HIV infection, antiretroviral treatment, ageing, and non-AIDS related morbidity. BMJ 338:a3172

  8. 8.

    Vachiat A, McCutcheon K, Tsabedze N, Zachariah D, Manga P (2017) HIV and ischemic heart disease. J Am Coll Cardiol 69:73–82

  9. 9.

    Manga P, McCutcheon K, Tsabedze N, Vachiat A, Zachariah D (2017) HIV and nonischemic heart disease. J Am Coll Cardiol 69:83–91

  10. 10.

    Bots ML, Hoes AW, Koudstaal PJ, Hofman A, Grobbee DE (1997) Common carotid intima-media thickness and risk of stroke and myocardial infarction: the Rotterdam Study. Circulation 96:1432–1437

  11. 11.

    Stein JH, Currier JS, Hsue PY (2014) Arterial disease in patients with human immunodeficiency virus infection: what has imaging taught us? JACC Cardiovasc Imaging 7:515–525

  12. 12.

    Lorenz MW, Polak JF, Kavousi M et al (2012) Carotid intima-media thickness progression to predict cardiovascular events in the general population (the PROG-IMT collaborative project): a meta-analysis of individual participant data. Lancet 379:2053–2062

  13. 13.

    Den Ruijter HM, Peters SA, Anderson TJ et al (2012) Common carotid intima-media thickness measurements in cardiovascular risk prediction: a meta-analysis. JAMA 308:796–803

  14. 14.

    van Vonderen MG, Smulders YM, Stehouwer CD et al (2009) Carotid intima-media thickness and arterial stiffness in HIV-infected patients: the role of HIV, antiretroviral therapy, and lipodystrophy. J Acquir Immune Defic Syndr 50:153–161

  15. 15.

    van Vonderen MG, Hassink EA, van Agtmael MA et al (2009) Increase in carotid artery intima-media thickness and arterial stiffness but improvement in several markers of endothelial function after initiation of antiretroviral therapy. J Infect Dis 199:1186–1194

  16. 16.

    Zahnd G, Vray D, Serusclat A et al (2012) Longitudinal displacement of the carotid wall and cardiovascular risk factors: associations with aging, adiposity, blood pressure and periodontal disease independent of cross-sectional distensibility and intima-media thickness. Ultrasound Med Biol 38:1705–1715

  17. 17.

    Svedlund S, Eklund C, Robertsson P, Lomsky M, Gan LM (2011) Carotid artery longitudinal displacement predicts 1-year cardiovascular outcome in patients with suspected coronary artery disease. Arterioscler Thromb Vasc Biol 31:1668–1674

  18. 18.

    El Jalbout R, Cloutier G, Roy Cardinal M-H et al (2019) The value of non-invasive vascular elastography (NIVE) in detecting early vascular changes in overweight and obese children. Eur Radiol 29:3854–3861

  19. 19.

    Cote AT, Phillips AA, Harris KC, Sandor GG, Panagiotopoulos C, Devlin AM (2015) Obesity and arterial stiffness in children: systematic review and meta-analysis. Arterioscler Thromb Vasc Biol 35:1038–1044

  20. 20.

    Zhu ZQ, Chen LS, Wang H et al (2019) Carotid stiffness and atherosclerotic risk: non-invasive quantification with ultrafast ultrasound pulse wave velocity. Eur Radiol 29:1507–1517

  21. 21.

    Shi H, Mitchell CC, McCormick M, Kliewer MA, Dempsey RJ, Varghese T (2008) Preliminary in vivo atherosclerotic carotid plaque characterization using the accumulated axial strain and relative lateral shift strain indices. Phys Med Biol 53:6377–6394

  22. 22.

    Naim C, Cloutier G, Mercure E et al (2013) Characterisation of carotid plaques with ultrasound elastography: feasibility and correlation with high-resolution magnetic resonance imaging. Eur Radiol 23:2030–2041

  23. 23.

    Hansen HH, de Borst GJ, Bots ML, Moll FL, Pasterkamp G, de Korte CL (2016) Validation of noninvasive in vivo compound ultrasound strain imaging using histologic plaque vulnerability features. Stroke 47:2770–2775

  24. 24.

    Roy Cardinal MH, Heusinkveld MHG, Qin Z et al (2017) Carotid artery plaque vulnerability assessment using noninvasive ultrasound elastography: validation with MRI. AJR Am J Roentgenol 209:142–151

  25. 25.

    Dempsey RJ, Varghese T, Jackson DC et al (2018) Carotid atherosclerotic plaque instability and cognition determined by ultrasound-measured plaque strain in asymptomatic patients with significant stenosis. J Neurosurg 128:111-119

  26. 26.

    Cloutier G, Roy Cardinal M-H, Ju Y, Giroux M-F, Lanthier S, Soulez G (2018) Carotid plaque vulnerability assessment using ultrasound elastography and echogenicity analysis. AJR Am J Roentgenol 211:847–855

  27. 27.

    Baker JV, Duprez D, Rapkin J et al (2009) Untreated HIV infection and large and small artery elasticity. J Acquir Immune Defic Syndr 52:25–31

  28. 28.

    Kaplan RC, Sinclair E, Landay AL et al (2011) T cell activation predicts carotid artery stiffness among HIV-infected women. Atherosclerosis 217:207–213

  29. 29.

    Karim R, Mack WJ, Kono N et al (2014) T-cell activation, both pre- and post-HAART levels, correlates with carotid artery stiffness over 6.5 years among HIV-infected women in the WIHS. J Acquir Immune Defic Syndr 67:349–356

  30. 30.

    Lekakis J, Ikonomidis I, Palios J et al (2009) Association of highly active antiretroviral therapy with increased arterial stiffness in patients infected with human immunodeficiency virus. Am J Hypertens 22:828–834

  31. 31.

    Durand M, Chartrand-Lefebvre C, Baril JG et al (2017) The Canadian HIV and aging cohort study—determinants of increased risk of cardio-vascular diseases in HIV-infected individuals: rationale and study protocol. BMC Infect Dis 17:611

  32. 32.

    Destrempes F, Meunier J, Giroux M-F, Soulez G, Cloutier G (2011) Segmentation of plaques in sequences of ultrasonic B-mode images of carotid arteries based on motion estimation and a Bayesian model. IEEE Trans Biomed Eng 58:2202–2211

  33. 33.

    Gamble G, Zorn J, Sanders G, MacMahon S, Sharpe N (1994) Estimation of arterial stiffness, compliance, and distensibility from M-mode ultrasound measurements of the common carotid artery. Stroke 25:11–16

  34. 34.

    Schmitt C, Soulez G, Maurice R, Giroux M, Cloutier G (2007) Noninvasive vascular elastography: toward a complementary characterization tool of atherosclerosis in carotid arteries. Ultrasound Med Biol 33:1841–1858

  35. 35.

    Maurice RL, Soulez G, Giroux MF, Cloutier G (2008) Noninvasive vascular elastography for carotid artery characterization on subjects without previous history of atherosclerosis. Med Phys 35:3436–3443

  36. 36.

    Mercure E, Destrempes F, Roy Cardinal MH et al (2014) A local angle compensation method based on kinematics constraints for non-invasive vascular axial strain computations on human carotid arteries. Comput Med Imaging Graph 38:123–136

  37. 37.

    Sheskin DJ (2011) Handbook of parametric and nonparametric statistical procedures, fifth edn. Chapman and Hall/CRC

  38. 38.

    Janjua SA, Staziaki PV, Szilveszter B et al (2017) Presence, characteristics, and prognostic associations of carotid plaque among people living with HIV. Circ Cardiovasc Imaging 10:e005777

  39. 39.

    Hanna DB, Moon JY, Haberlen SA et al (2018) Carotid artery atherosclerosis is associated with mortality in HIV-positive women and men. AIDS 32:2393–2403

  40. 40.

    O’leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK Jr (1999) Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. N Engl J Med 340:14–22

  41. 41.

    Inaba Y, Chen JA, Bergmann SR (2012) Carotid plaque, compared with carotid intima-media thickness, more accurately predicts coronary artery disease events: a meta-analysis. Atherosclerosis 220:128–133

  42. 42.

    Hass WK, Fields WS, North RR, Kircheff II, Chase NE, Bauer RB (1968) Joint study of extracranial arterial occlusion. II. Arteriography, techniques, sites, and complications. JAMA 203:961–968

  43. 43.

    Zarins CK, Giddens DP, Bharadvaj BK, Sottiurai VS, Mabon RF, Glagov S (1983) Carotid bifurcation atherosclerosis. Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ Res 53:502–514

  44. 44.

    Crisby M, Nordin-Fredriksson G, Shah PK, Yano J, Zhu J, Nilsson J (2001) Pravastatin treatment increases collagen content and decreases lipid content, inflammation, metalloproteinases, and cell death in human carotid plaques: implications for plaque stabilization. Circulation 103:926–933

  45. 45.

    Nayak R, Schifitto G, Doyley MM (2018) Visualizing angle-independent principal strains in the longitudinal view of the carotid artery: phantom and in vivo evaluation. Ultrasound Med Biol 44:1379–1391

Download references

Funding

This study was initiated through the support of the Canadian Institute of Health Research (CIHR, Canadian HIV and Aging Cohort Study, group grant no. 284512); it is now supported by CIHR group grant no. 398643 and project grant no. 399544.

Author information

Correspondence to Guy Cloutier.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Dr. Guy Cloutier.

Conflict of interest

The authors declare that they have no conflict of interest.

Statistics and biometry

Co-authors (MHRC, GS, and GC) have significant statistical expertise.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional review board approval was obtained.

Methodology

• prospective

• cross-sectional study

• performed at one institution

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 34 kb).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Roy Cardinal, M., Durand, M., Chartrand-Lefebvre, C. et al. Increased carotid artery wall stiffness and plaque prevalence in HIV infected patients measured with ultrasound elastography. Eur Radiol (2020). https://doi.org/10.1007/s00330-020-06660-9

Download citation

Keywords

  • HIV infections
  • Premature aging
  • Ultrasonography
  • Carotid arteries
  • Elasticity imaging techniques