(Radiology. 1999;213:167-172.)
© RSNA, 1999
Asymptomatic Carotid Arterial Disease in Young Patients following Neck Radiation Therapy for Hodgkin Lymphoma1
Leonard J. King, MRCP, FRCR,
Salma N. Hasnain, DCR(R), DMU, MSc,
Judith A. W. Webb, MD, FRCP, FRCR,
Judith E. Kingston, FRCP,
Elizabeth A. Shafford, MRCP,
T. Andrew Lister, MD, FRCP, FRCPath,
Jonathan Shamash, MD, MRCP and
Rodney H. Reznek, FRCP, FRCR
1 From the Departments of Radiology (L.J.K., S.N.H., J.A.W.W., R.H.R.), Oncology (T.A.L., J.S.), and Pediatric Oncology (J.E.K., E.A.S.), St Bartholomew's Hospital, London, England. From the 1997 RSNA scientific assembly. Received May 27, 1998; revision requested July 16; final revision received January 25, 1999; accepted March 30. Address reprint requests to L.J.K., Department of Radiology, Royal Hospital Haslar, Gosport, Hampshire, PO12 2AA, United Kingdom.
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Abstract
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PURPOSE: To determine the prevalence and severity of asymptomatic carotid arterial disease in young patients following neck radiation therapy for Hodgkin lymphoma and to compare the prevalence of carotid arterial disease following radiation therapy alone with that following radiation therapy and chemotherapy.
MATERIALS AND METHODS: Forty-two survivors of childhood or early adult Hodgkin lymphoma aged 18–37 years who had undergone radiation therapy more than 5 years earlier underwent carotid arterial ultrasonography. Common carotid intima-media thickness was measured; carotid vessels were assessed for intima-media abnormalities. Results were compared with those from 33 control subjects.
RESULTS: Patients had a significantly greater number of abnormal scans than did control subjects (11 [26%] vs one [3%]; P < .01). Ten patients (24%) had intima-media abnormalities that did not cause significant stenosis; one patient had diffuse bilateral intima-media thickening (mean, 1.99 mm) with greater than 70% stenosis of both common carotid arteries. Intima-media thickness was significantly greater in patients (0.51 mm) than in control subjects (0.43 mm; P < .005). The number of abnormalities in patients with radiation therapy plus chemotherapy (six [19%] of 31 patients) did not differ significantly from the number in patients with only radiation therapy (five [45%] of 11 patients; P = .12); there was no significant difference between median intima-media thicknesses (0.50 mm vs 0.51 mm, P > .2).
CONCLUSION: Asymptomatic carotid arterial disease occurs frequently in young patients following neck radiation therapy for Hodgkin lymphoma. No difference in prevalence was shown between only radiation therapy and radiation therapy plus chemotherapy.
Index terms: Carotid arteries, abnormalities, 904.47 • Carotid arteries, stenosis or obstruction, 904.47, 904.7212 • Carotid arteries, US, 904.1298 • Hodgkin disease, 99.8342 • Radiations, injurious effects, complications of therapeutic radiology, 904.126, 904.47, 904.7212
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Introduction
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Radiation therapy has been implicated by several studies as a causal factor in the development of early and atypical carotid arterial disease. Most previous studies have concentrated on symptomatic carotid arterial disease (1–10), often in older patients and commonly following high-dose radiation therapy for head and neck cancers (1,4,6,8,9,1,4,6,8, 9, 11–17). A small number of patients with symptomatic carotid arterial disease following radiation therapy to the neck for treatment of lymphoma have been reported on, which suggests that these patients are also predisposed to early carotid arterial disease (5,6,12,16,18,19).
Previously, Elerding et al (11), who used the noninvasive techniques carotid phonoangiography and oculoplethysmography for detecting turbulent blood flow, demonstrated hemodynamically significant abnormalities in 12 (16%) of 77 patients and non–hemodynamically significant abnormalities in five (6%) of 77 patients who had received radiation therapy for Hodgkin disease; eight of the 77 patients were symptomatic (11).
Duplex ultrasonography (US) has previously been used to assess carotid arterial disease following radiation therapy for head and neck cancer (14,15), but to our knowledge the prevalence and severity of asymptomatic carotid arterial disease in young patients following radiation therapy to the neck for lymphoma has not been previously investigated with carotid arterial US. We performed this study to determine the prevalence and severity of asymptomatic carotid arterial disease in young patients following neck radiation therapy for Hodgkin lymphoma and to compare the prevalence of carotid arterial disease following radiation therapy alone with that following radiation therapy and chemotherapy.
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MATERIALS AND METHODS
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Patients and Control Subjects
Between November 1995 and March 1997, US of the carotid artery was performed in 42 long-term survivors (age range, 18–37 years) of childhood or early adult Hodgkin lymphoma who had received radiation therapy to the neck. All patients were in remission and asymptomatic, with no history of previous stroke or transient ischemic attack. A control group of 33 healthy volunteers (age range, 23–36 years) also underwent US.
All patients and control subjects completed a questionnaire to assess their cardiovascular risk factors; had their height, weight, and blood pressure measured; and provided a blood sample following an overnight fast for measurement of lipid levels. Smoking history was assessed in pack-years. No patients or control subjects had a known history of sickle cell disease, arteritis, or diabetes mellitus (type 1 or 2), and urinalysis was performed to exclude glucosuria. A positive family history of cerebrovascular or cardiovascular disease was defined as a cerebral or cardiac ischemic event in a first-degree relative younger than 65 years.
Technique
All scans were obtained with a model 128/XP10 US scanner (Acuson, Mountain View, Calif) by one of two observers (L.J.K. or S.N.H.) by using a 7.5-MHz linear-array transducer and standardized machine settings in a preset carotid arterial imaging program. Patients were examined in the supine position with the neck extended.
US of both common carotid arteries and the proximal portions of the internal and external carotid arteries was performed in the longitudinal and transverse planes. The intima-media thickness was defined as the distance between the echogenic line representing the blood-intima interface and the echogenic line representing the media-adventitia interface (Fig 1). The intima-media thickness was always measured on the posterior wall of the common carotid artery in the longitudinal plane by using an anterolateral approach, with the transducer head perpendicular to the vessel. Measurements of the intima-media thickness were performed on magnified, static images with electronic calipers. The intima-media thickness was recorded three times at each of six sites: the proximal, middle, and distal sections of both common carotid arteries. The mean intima-media thickness was calculated.
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Figure 1. Longitudinal US image of the common carotid artery in a healthy 30-year-old male volunteer. The intima-media thickness is depicted by the arrows. Electronic calipers used to measure the intima-media thickness are also displayed.
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The proximal measurements were obtained in the lowest clearly visualized segment of each common carotid artery, with the transducer in the supraclavicular region. The distal measurements were obtained between 0.5 and 1.0 cm from the carotid arterial bifurcation, and the measurements in the middle portion of the common carotid artery were obtained approximately halfway between the proximal and distal measurements. The vessel wall at the carotid arterial bifurcation and in the proximal portions of the internal and external carotid arteries was also subjectively assessed, although measurements of the intima-media thickness were not recorded at these sites due to difficulty in obtaining consistent images with the vessel wall perpendicular to the ultrasound beam.
A color and spectral Doppler examination of the extracranial carotid vessels was also performed, and flow velocities were recorded at multiple points in each vessel. The proximal and middle sections of both vertebral arteries were assessed in the longitudinal plane for the presence of antegrade flow, away from the transducer at color Doppler US. Hard-copy images and a VHS video recording (Panasonic AG-6200; Matsushita Electric Trading, Osaka, Japan) were obtained for each examination.
Magnetic resonance (MR) angiography was also performed in one patient for confirmation of the US appearances by using a 1.5-T imager (Signa; GE Medical Systems, Milwaukee, Wis). A two-dimensional time-of-flight examination with flow compensation was performed by using the following parameters: 41/5 (repetition time msec/echo time msec); flip angle, 60°; matrix, 256 x 128; one signal acquired; and section thickness, 1.5 mm.
Analysis
Abnormalities of the intima-media complex identified on US scans were classified by using the noninvasive US arterial biopsy classification described by Belcaro et al (Table 1) (20). Degree of vessel stenosis was assessed by measuring the percentage reduction in luminal diameter on transverse images and by analyzing the associated flow velocity changes. When multiple abnormalities were identified in an individual subject, they were classified by the highest grade lesion.
The median intima-media thicknesses and numbers of abnormal scans in the patient and control groups were compared. In addition, the median intima-media thicknesses and numbers of abnormal scans in patients who had received chemotherapy and radiation therapy were compared with those in patients who had received only radiation therapy, and 20–29-year-old patients were compared with 30–39-year-old patients.
Statistical analysis was performed with a personal computer by using a commercially available software package (SPSS version 6.13 for Windows; SPSS, Chicago, Ill). Median intima-media thicknesses were compared by using the Mann-Whitney U test, and the numbers of abnormal scans were compared by using the Fisher exact test. Comparison of the mean age, body mass index, blood pressure, lipid levels, and pack-years of smoking between the study and control groups was performed with a Student t test. The numbers of men and women and family histories of cardiovascular or cerebrovascular disease were compared between the two groups by using the 
2 test.
To assess the repeatability of intima-media thickness measurements, the intima-media thicknesses in a subgroup of eight control subjects were measured independently by both observers. The intima-media thickness measurements were then repeated by both observers at a later date, and the interobserver and intraobserver coefficients of variation were calculated.
The research protocol was approved by the East London and City Health Authority Research Ethics Committee, and informed consent was obtained from all subjects.
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RESULTS
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Patients and Control Subjects
The age at diagnosis in the patient group ranged from 4 to 29 years (mean age, 13 years). Total therapeutic radiation doses received by the patient group ranged from 2,250 to 4,000 cGy and were delivered in 15–25 fractions. All patients had received treatment more than 5 years earlier (range, 5.1–22.8 years; mean, 13 years). Eleven patients (26%) had received radiation therapy alone, and 31 (74%) had received a combination of radiation therapy and chemotherapy. A standard mantle radiation therapy port had been used that extended up to the skull base; thus, both common carotid arteries and the origins of the internal and external carotid arteries were included within the radiation field.
The mean age in the control group (29 years) was slightly higher than that in the study group (27 years), but there was no significant difference between the two groups in the sex distribution, smoking habits, or number of first-degree relatives with a history of cerebrovascular or cardiovascular disease (Table 2). In addition, there were no significant differences in the mean values for body mass index, blood pressure, or lipid levels between the study and control groups (Table 3).
Good repeatability of intima-media thickness measurement was demonstrated with low intraobserver coefficients of variation of 3.1% and 2.5% for each observer and a low interobserver coefficient of variation of 4.2%.
US Findings
There were significantly more abnormal scans in the study group (11 [26%] of 42 patients) than in the control group (one [3%] of 33 control subjects), and the median intima-media thickness was greater in the study group (0.51 mm) than in the control group (0.43 mm) (Table 4).
The US arterial biopsy classifications of the abnormalities detected in the study group are shown in Table 5. One patient had an US arterial biopsy class V abnormality on a scan, with diffuse plaque and intima-media thickening in the common carotid arteries (mean thickness, 1.99 mm) and a reduction in luminal diameter of greater than 70% bilaterally. Spectral analysis demonstrated generalized bilateral spectral broadening and elevated peak systolic flow velocities of up to 2.6 msec-1. The US appearances were later confirmed with MR angiography (Fig 2).
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Figure 2a. Images obtained in a 36-year-old man 10 years after radiation therapy for Hodgkin lymphoma. The patient had no previous history of vasculitis, normal serial erythrocyte sedimentation rate measurements, normal upper limb pulses, normal femoral arteries, and no substantial cardiovascular risk factors except a slightly elevated cholesterol level. (a) Longitudinal US image of the left common carotid artery shows diffuse thickening of the intima-media (cursors), which measures 2.8 mm. This thickening caused significant stenosis (class V abnormality), with reduction of the luminal diameter of 2 mm (arrows). (b) Longitudinal US image of the proximal section of the right common carotid artery in the same patient shows irregular thickening of the intima-media (straight arrows), with a significant proximal stenosis (curved arrow). (c) Transverse US image of the right common carotid artery at the point of maximum stenosis (arrows) shows circumferential thickening of the intima-media. (d) Two-dimensional time-of-flight MR angiogram (41/5; flip angle, 60°) confirms the US findings of diffuse narrowing of the left common carotid artery (arrowheads) and shows less marked diffuse narrowing of the right common carotid artery, with a tight focal proximal stenosis (solid arrow). The normal vertebral arteries (open arrows) also are shown.
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Figure 2b. Images obtained in a 36-year-old man 10 years after radiation therapy for Hodgkin lymphoma. The patient had no previous history of vasculitis, normal serial erythrocyte sedimentation rate measurements, normal upper limb pulses, normal femoral arteries, and no substantial cardiovascular risk factors except a slightly elevated cholesterol level. (a) Longitudinal US image of the left common carotid artery shows diffuse thickening of the intima-media (cursors), which measures 2.8 mm. This thickening caused significant stenosis (class V abnormality), with reduction of the luminal diameter of 2 mm (arrows). (b) Longitudinal US image of the proximal section of the right common carotid artery in the same patient shows irregular thickening of the intima-media (straight arrows), with a significant proximal stenosis (curved arrow). (c) Transverse US image of the right common carotid artery at the point of maximum stenosis (arrows) shows circumferential thickening of the intima-media. (d) Two-dimensional time-of-flight MR angiogram (41/5; flip angle, 60°) confirms the US findings of diffuse narrowing of the left common carotid artery (arrowheads) and shows less marked diffuse narrowing of the right common carotid artery, with a tight focal proximal stenosis (solid arrow). The normal vertebral arteries (open arrows) also are shown.
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Figure 2c. Images obtained in a 36-year-old man 10 years after radiation therapy for Hodgkin lymphoma. The patient had no previous history of vasculitis, normal serial erythrocyte sedimentation rate measurements, normal upper limb pulses, normal femoral arteries, and no substantial cardiovascular risk factors except a slightly elevated cholesterol level. (a) Longitudinal US image of the left common carotid artery shows diffuse thickening of the intima-media (cursors), which measures 2.8 mm. This thickening caused significant stenosis (class V abnormality), with reduction of the luminal diameter of 2 mm (arrows). (b) Longitudinal US image of the proximal section of the right common carotid artery in the same patient shows irregular thickening of the intima-media (straight arrows), with a significant proximal stenosis (curved arrow). (c) Transverse US image of the right common carotid artery at the point of maximum stenosis (arrows) shows circumferential thickening of the intima-media. (d) Two-dimensional time-of-flight MR angiogram (41/5; flip angle, 60°) confirms the US findings of diffuse narrowing of the left common carotid artery (arrowheads) and shows less marked diffuse narrowing of the right common carotid artery, with a tight focal proximal stenosis (solid arrow). The normal vertebral arteries (open arrows) also are shown.
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Figure 2d. Images obtained in a 36-year-old man 10 years after radiation therapy for Hodgkin lymphoma. The patient had no previous history of vasculitis, normal serial erythrocyte sedimentation rate measurements, normal upper limb pulses, normal femoral arteries, and no substantial cardiovascular risk factors except a slightly elevated cholesterol level. (a) Longitudinal US image of the left common carotid artery shows diffuse thickening of the intima-media (cursors), which measures 2.8 mm. This thickening caused significant stenosis (class V abnormality), with reduction of the luminal diameter of 2 mm (arrows). (b) Longitudinal US image of the proximal section of the right common carotid artery in the same patient shows irregular thickening of the intima-media (straight arrows), with a significant proximal stenosis (curved arrow). (c) Transverse US image of the right common carotid artery at the point of maximum stenosis (arrows) shows circumferential thickening of the intima-media. (d) Two-dimensional time-of-flight MR angiogram (41/5; flip angle, 60°) confirms the US findings of diffuse narrowing of the left common carotid artery (arrowheads) and shows less marked diffuse narrowing of the right common carotid artery, with a tight focal proximal stenosis (solid arrow). The normal vertebral arteries (open arrows) also are shown.
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Ten patients (24%) had focal or generalized abnormalities of the intima-media, such as discontinuity, irregularity, focal thickening, or early plaque formation in the common carotid or proximal sections of the internal carotid arteries, which did not cause significant stenosis (US arterial biopsy class II or III abnormalities) (Figs 3, 4).
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Figure 3a. US images obtained in two patients show class III carotid arterial abnormalities following radiation therapy. (a) Diffuse thickening and irregularity of the intima-media (arrows) in the distal section of the common carotid artery extend into the proximal section of the internal carotid artery in a 25-year-old man 17 years after treatment. (b) Electronic calipers outline a 2-mm-thick focal plaque at the carotid arterial bifurcation in a 37-year-old man 11 years after treatment.
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Figure 3b. US images obtained in two patients show class III carotid arterial abnormalities following radiation therapy. (a) Diffuse thickening and irregularity of the intima-media (arrows) in the distal section of the common carotid artery extend into the proximal section of the internal carotid artery in a 25-year-old man 17 years after treatment. (b) Electronic calipers outline a 2-mm-thick focal plaque at the carotid arterial bifurcation in a 37-year-old man 11 years after treatment.
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Figure 4a. US images obtained in two patients with subtle class II abnormalities of the intima-media. (a) Focal loss of the blood-intima interface (arrowheads) in the middle part of the common carotid artery in a 33-year-old woman 13 years after radiation therapy. (b) Common carotid artery in a 30-year-old man 17 years after treatment shows diffuse interruption and irregularity of the blood-intima interface (arrows). In a and b, the electronic calipers were used to measure the intima-media thickness on the posterior wall.
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Figure 4b. US images obtained in two patients with subtle class II abnormalities of the intima-media. (a) Focal loss of the blood-intima interface (arrowheads) in the middle part of the common carotid artery in a 33-year-old woman 13 years after radiation therapy. (b) Common carotid artery in a 30-year-old man 17 years after treatment shows diffuse interruption and irregularity of the blood-intima interface (arrows). In a and b, the electronic calipers were used to measure the intima-media thickness on the posterior wall.
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There was no significant difference in the number of abnormal scans between the patients who had undergone radiation therapy plus chemotherapy (six [19%] of 31 patients) and the patients who had undergone only radiation therapy (five [45%] of 11 patients; P = .12). No significant difference was found in the median intima-media thickness between patients who had received radiation therapy and chemotherapy (0.50 mm) and patients who had received only radiation therapy (0.51 mm; P > .2).
Significantly fewer patients aged 20–29 years (four [13%] of 30 patients) than patients aged 30–39 years (seven [64%] of 11 patients) had detectable abnormalities (P < .005). There was no significant difference, however, in the median intima-media thickness between 20–29-year-old patients (0.50 mm) and 30–39-year-old patients (0.51 mm; P > .5).
One control subject had class II abnormalities of the intima-media complex in the distal sections of the common carotid arteries and the proximal sections of the internal carotid arteries. No other extracranial carotid arterial abnormalities were detected in the control group.
Antegrade blood flow was demonstrated in the vertebral arteries of all patients and control subjects.
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DISCUSSION
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The prevalence of atheromatous change in the carotid arteries increases with patient age. In our study, patients younger than 40 years, who would be expected under normal circumstances to have a low prevalence of carotid arterial disease, were examined. Belcaro et al (20) have reported abnormalities at carotid and femoral arterial US in only two (0.8%) of 250 healthy volunteers aged 20–29 years and in 72 (28.8%) of 250 healthy volunteers aged 30–39 years, none of whom had plaques causing more than 50% stenosis.
In our study, we identified carotid arterial abnormalities in 13% of 20–29-year-old patients and in 64% of 30–39-year-old patients following radiation therapy treatment to the neck for childhood or early adult lymphoma; these percentages were significantly higher than those in the control group. In most cases, the abnormalities identified were minor changes of the intima-media that did not cause significant carotid arterial stenosis, although one patient did have severe bilateral common carotid arterial disease. The atypical changes identified in this one patient caused us to consider other forms of vascular disease; however, there was no previous history of vasculitis, the patient had normal serial erythrocyte sedimentation rates, normal upper limb pulses, normal femoral arteries at US examination, and no cardiovascular risk factors, other than a slightly elevated cholesterol level at 6.2 mmol/L. The intima-media thickness in our patients was also significantly larger than that in the control subjects.
Belcaro et al (20) devised the US scale to classify atheromatous carotid disease rather than post–radiation therapy changes; however, they provided a useful template for the subjective analysis of the intima-media, as well as a baseline of normality in young subjects that concurs with our own control data. While we recognize that the pathogenesis of the abnormalities identified in this study may be variable and different from that of carotid atheromatous disease, most of the abnormalities we identified in patients after radiation therapy were similar to those previously described in subjects who did not undergo radiation therapy (20).
The overall prevalence of carotid arterial abnormalities in our study (11 [26%] of 42 patients) is comparable to the data published by Elerding et al (11), who used carotid phonoangiography and oculoplethysmography. They reported abnormalities in 17 (22%) of 77 patients, all of whom had undergone radiation therapy more than 5 years earlier for Hodgkin lymphoma, with a mean age at treatment of 28 years.
The number of hemodynamically significant abnormalities reported in this previous study (12 [16%] of 77 patients) was not borne out in our study, in which we have identified a significant carotid arterial stenosis in only one (2%) of the 42 patients. Elerding et al (11), however, included eight symptomatic patients in their study, whereas all our patients were asymptomatic; this probably accounts for the difference. It is also likely that several of the abnormalities detected in our study, such as discontinuity or irregularity of the intima-media, would give normal results with the noninvasive methods used by Elerding et al, as these abnormalities were not associated with turbulent arterial flow at Doppler US. Thus, Elerding et al may have underestimated the number of patients with carotid arterial abnormalities by using the carotid phonoangiographic and oculoplethysmographic techniques.
No significant differences were identified between those patients who had received only radiation therapy and those who had received radiation therapy and chemotherapy. This suggests that chemotherapy is not an additional risk factor for the development of carotid arterial disease, although our patient with bilateral carotid arterial stenoses had received a combination of radiation therapy and chemotherapy.
The importance of the minor changes described in this group of young patients after radiation therapy is not known, and a long-term follow-up study in such patients is required to determine whether the minor intima-media abnormalities and plaques identified predispose these patients to the development of significant stenotic lesions. A longitudinal study to assess the progression and long-term importance of the abnormalities identified would also be helpful in determining whether screening and long-term follow-up carotid arterial US examinations in these patients is justified.
The treatment implications for radiation therapy in patients with early carotid arterial disease are also unclear without further data on the long-term stability and progression of these lesions. Monitoring risk factors for atherosclerosis such as plasma lipid levels and blood pressure in patients with identifiable abnormalities, however, seems prudent. Asymptomatic patients with more severe carotid arterial disease, such as the patient in our study with bilateral common carotid arterial stenoses, will provide clinicians with a management dilemma in which the risks of progression and stroke have to be weighed against the risks of surgical intervention.
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Acknowledgments
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We thank Janice M. Thomas, MSc, DIC, FSS, for her for assistance with the statistical analysis of our data.
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Footnotes
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Author contributions: Guarantors of integrity of entire study, L.J.K., R.H.R.; study concepts and design, L.J.K., R.H.R., J.A.W.W.; definition of intellectual content, L.J.K., R.H.R.; literature research, L.J.K.; clinical studies, E.A.S., J.E.K., J.S., T.A.L.; data acquisition, L.J.K., S.N.H.; data analysis, L.J.K., R.H.R., J.A.W.W.; statistical analysis, L.J.K.; manuscript preparation, L.J.K.; manuscript editing, R.H.R., J.A.W.W.; manuscript review, E.A.S., J.E.K., T.A.L., J.S.
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Abstract
Introduction
