Introduction
The risk for atherosclerosis can be measured according to the quantity and nature of the disease using different modalities, such as coronary calcium scoring and computed tomographic angiography and ultrasound of the carotid and femoral arteries. Ultrasound can characterize atheroma without radiation and identify markers of increased cardiovascular (CV) risk such as increased intima-media thickness (IMT) and plaque thickness, calcification, stenosis, and lucency.
1- Pignoli P.
- Tremoli E.
- Poli A.
- Oreste P.
- Paoletti R.
Intimal plus medial thickness of the arterial wall: a direct measurement with ultrasound imaging.
, 2Ultrasonographically assessed carotid morphology and the risk of coronary artery disease.
, 3- O'Leary D.H.
- Polak J.F.
- Kronmal R.A.
- Manolio T.A.
- Burke G.L.
- Wolfson Jr., S.K.
Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group.
, 4- Grønholdt M.L.M.
- Wiebe B.M.
- Laursen H.
- Nielsen T.G.
- Schroeder T.V.
- Sillesen H.
Lipid-rich carotid artery plaques appear echolucent on ultrasound B-mode images and may be associated with intraplaque haemorrhage.
, 5- Belcaro G.
- Barsotti A.
- Nicolaides A.N.
“Ultrasonic biopsy”—a non-invasive screening technique to evaluate the cardiovascular risk and to follow up the progression and the regression of arteriosclerosis.
Ultrasound biopsy and
biomicroscopy are terms that describe how ultrasound can reveal fine details of the arterial intima-media complex (IMC),
5- Belcaro G.
- Barsotti A.
- Nicolaides A.N.
“Ultrasonic biopsy”—a non-invasive screening technique to evaluate the cardiovascular risk and to follow up the progression and the regression of arteriosclerosis.
especially at high frequency.
6- Osika W.
- Dangardt F.
- Grönros J.
- Lundstam U.
- Myredal A.
- Johansson M.
- et al.
Increasing peripheral artery intima thickness from childhood to seniority.
,7- Johansson M.
- Myredal A.
- Friberg P.
- Gan L.M.
High-resolution ultrasound showing increased intima and media thickness of the radial artery in patients with end-stage renal disease.
These include breaks in the continuity of the normally smooth echogenic intima-blood interface and clouding or granularity of the normally lucent middle layer that is associated with the media.
5- Belcaro G.
- Barsotti A.
- Nicolaides A.N.
“Ultrasonic biopsy”—a non-invasive screening technique to evaluate the cardiovascular risk and to follow up the progression and the regression of arteriosclerosis.
In this report we describe another ultrasound finding that to our knowledge is novel and consists of a long, mobile, strandlike structure that trails downstream from its anchor at the common carotid artery (CCA)–bulb margin. Three cases of this finding are derived from a CV health screening program. Follow-up images in one case suggest that strands and atherogenesis may be associated.
Discussion
We describe the two-dimensional ultrasound finding of strandlike mobile structures that trailed distally from the CCA-bulb junction in three subjects at risk for or with known atherosclerosis. The strands were subtle and contiguous with either the intima or media. The development of new sessile material in the bulb of one subject that disappeared after initiation of a statin suggests the possibility of atheroma regression. Thrombus disappearance is another possibility, though anticoagulant or antiplatelet medication was not administered. Our cases suggest that carotid ultrasound strands are associated with atheroma and possibly atherogenesis.
The precise histology of the carotid strands we detected is unknown. One possibility is that the strands are fibrin filaments. Another possibility is that strands represent a lifting of the intima-associated layer of the very proximal bulb. The continuity of strands with the surface of the IMC is most evident on the images for cases 2 and 3. Strands may be a marker of the disruption of the IMC that tends to occur when CV risk factors are present. Electronic microscopic examination of carotid plaque may show detachment or absence of the endothelium on the basal lamina and cellular infiltration,
8- Congiu T.
- Schembri L.
- Tozzi M.
- Guasti L.
- Maio R.C.
- Cosentino M.
- et al.
Scanning electron microscopy examination of endothelium morphology in human carotid plaques.
which may reveal the thrombogenic subendothelium.
9- Rohl S.
- Eriksson L.
- Saxelin R.
Noninvasive in vivo assessment of the re-endothelialization process using ultrasound biomicroscopy in the rat carotid artery balloon injury model.
The location of the strands may also relate to flow disturbances and eddies associated with widening of the carotid artery at the start of the bulb.
10- Davies P.F.
- Shi C.
- DePaola N.
- Helmke B.P.
- Polacek D.C.
Hemodynamics and the focal origin of atherosclerosis.
Carotid strands may be easily overlooked during the usual focus on the presence or absence of plaque and stenosis. Detection of the strand in the first case was unexpected but primed us to search for this finding in other subjects.
Images were acquired by a registered vascular sonographer at the highest possible transducer frequency and were optimized for clarity according to recommended standards. Harmonic imaging was not used and may not have been helpful because of its decreased axial resolution compared with fundamental imaging. The normal carotid ultrasound examination generates an image with a double-line pattern that consists of a continuous echogenic intima-associated surface layer and adventitia layer sandwiching the lucent media and an IMT that is generally <1 mm.
1- Pignoli P.
- Tremoli E.
- Poli A.
- Oreste P.
- Paoletti R.
Intimal plus medial thickness of the arterial wall: a direct measurement with ultrasound imaging.
,5- Belcaro G.
- Barsotti A.
- Nicolaides A.N.
“Ultrasonic biopsy”—a non-invasive screening technique to evaluate the cardiovascular risk and to follow up the progression and the regression of arteriosclerosis.
Increased carotid IMT has been widely used as a marker of increased CV risk.
2Ultrasonographically assessed carotid morphology and the risk of coronary artery disease.
,3- O'Leary D.H.
- Polak J.F.
- Kronmal R.A.
- Manolio T.A.
- Burke G.L.
- Wolfson Jr., S.K.
Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group.
In addition to increased IMT, Belcaro
et al.5- Belcaro G.
- Barsotti A.
- Nicolaides A.N.
“Ultrasonic biopsy”—a non-invasive screening technique to evaluate the cardiovascular risk and to follow up the progression and the regression of arteriosclerosis.
described early changes in these layers in subjects at greater risk for CV events that include breaks in the normally continuous intima-blood interface and increased echogenicity or granularity of the media-adventitia layer. These findings were variably evident in our images and have also been described in other reports. For example, increased grayscale abnormality or inhomogeneity of this layer was found in a pediatric population with heterozygous familial hypercholesterolemia
11- Noto N.
- Okada T.
- Abe Y.
- Miyashita M.
- Kanamaru H.
- Karasawa K.
- et al.
Changes in the textural characteristics of intima-media complex in young patients with familial hypercholesterolemia: implication for visual inspection on B-mode ultrasound.
and adults with coronary artery disease.
12- Sandrock M.
- Cheng D.C.
- Schmitz D.
- Schmidt-Trucksass A.
Quantification of the wall inhomogeneity in B-mode sonographic images of the carotid artery.
We also noted evidence of IMC disruption in terms of variable breaks in or disappearance of the bright intima layer and granularity or clouding of the media.
Conventional 5- to 15-MHz ultrasound probes
2Ultrasonographically assessed carotid morphology and the risk of coronary artery disease.
,3- O'Leary D.H.
- Polak J.F.
- Kronmal R.A.
- Manolio T.A.
- Burke G.L.
- Wolfson Jr., S.K.
Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group.
enable measurement of IMT but not the individual components of the IMC. The advent of very high frequency imaging at 55 to 70 MHz enables separate measurement of the thickness of the intima and media so that changes can be detected and monitored in vivo.
6- Osika W.
- Dangardt F.
- Grönros J.
- Lundstam U.
- Myredal A.
- Johansson M.
- et al.
Increasing peripheral artery intima thickness from childhood to seniority.
,13- Dangardt F.
- Charakida M.
- Chiesa S.
- Bhowruth D.
- Rapala A.
- Thurn D.
- et al.
Intimal and medial arterial changes defined by ultra-high-frequency ultrasound: response to changing risk factors in children with chronic kidney disease.
Previously, microscopy of excised specimens was needed to visualize the IMC in fine detail. Histologic studies showed an association between radial artery intima hyperplasia and CV risk factors
14- Ruengsakulrach P.
- Sinclair R.
- Komeda M.
- Raman J.
- Gordon I.
- Buxton B.
Comparative histopathology of radial artery versus internal thoracic artery and risk factors for development of intimal hyperplasia and atherosclerosis.
and increased coronary artery intima hyperplasia and extracellular fat and macrophage infiltration.
15- Nakashima Y.
- Fujii H.
- Sumiyoshi S.
- Wight T.N.
- Sueishi K.
Early human atherosclerosis accumulation of lipid and proteoglycans in intimal thickenings followed by macrophage infiltration.
The original high-frequency ultrasound study by Osika
et al.6- Osika W.
- Dangardt F.
- Grönros J.
- Lundstam U.
- Myredal A.
- Johansson M.
- et al.
Increasing peripheral artery intima thickness from childhood to seniority.
showed a strong and separate association between peripheral arterial intima and media thickness with age. Osika
et al. also found increased radial artery intima thickness in patients with peripheral artery disease.
6- Osika W.
- Dangardt F.
- Grönros J.
- Lundstam U.
- Myredal A.
- Johansson M.
- et al.
Increasing peripheral artery intima thickness from childhood to seniority.
Increased radial artery intima and media thickness also occurs in dialysis patients.
7- Johansson M.
- Myredal A.
- Friberg P.
- Gan L.M.
High-resolution ultrasound showing increased intima and media thickness of the radial artery in patients with end-stage renal disease.
In a follow-up study, Dangardt
et al.13- Dangardt F.
- Charakida M.
- Chiesa S.
- Bhowruth D.
- Rapala A.
- Thurn D.
- et al.
Intimal and medial arterial changes defined by ultra-high-frequency ultrasound: response to changing risk factors in children with chronic kidney disease.
found that increased carotid media thickness in children with chronic renal failure decreased 1 year after renal transplantation.
Our images were obtained using an 8- to 10-MHz transducer. Imaging with a higher frequency probe may have demonstrated the strands more clearly and may have yielded additional insights. However, general application of very high frequency ultrasound is limited by its reduced tissue penetration. This would be more of an issue in adults and obese subjects.
13- Dangardt F.
- Charakida M.
- Chiesa S.
- Bhowruth D.
- Rapala A.
- Thurn D.
- et al.
Intimal and medial arterial changes defined by ultra-high-frequency ultrasound: response to changing risk factors in children with chronic kidney disease.
Other modalities that can generate very high resolution images are invasive, such as optical coherence tomography and intravascular ultrasound. The prevalence of the strands we describe is not known. Strands are a subtle finding that can be easily overlooked. Awareness of the possibility of carotid artery strands may enable additional study of this finding in the future.
Article Info
Publication History
Published online: July 17, 2020
Footnotes
Conflicts of interest: The authors reported no actual or potential conflicts of interest relative to this document.
Copyright
2020 by the American Society of Echocardiography. Published by Elsevier Inc.