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Evaluation of lingual artery hemodynamics in stroke patients using Doppler ultrasound
Evaluation of lingual artery hemodynamics in stroke patients using Doppler ultrasound Daniel NEW
E. Myers, D.D.S., YORK
UNIVERSITY
Sanders Davis,
INSTITUTE
M.D.,
OF REHABILITATION
and June N. Barker,
Ph.D.,
New York, N, Y,
MEDICINE
Doppler blood flow studies were carried out on deep lingual arteries of young adults and stroke patients to see how the hemodynamics of this artery would be altered in the stroke group, who were selected on the basis of their having carotid atherosclerosis. The healthy controls exhibited a consistent and characteristic velocity pulse profile, which included a distinctive dichrotic notch and significant diastolic flow. The stroke group especially lacked these two critical parameters, and some exhibited amorphous flow patterns and cardiac arrhythmias. Implications of these findings in relationship to atherosclerosis are discussed.
W
ith the advent of inexpensive, accurate, and noninvasive methods for clinical blood flow studies, the role of hemodynamic disturbances in systemic disease processes can be investigated. Of particular interest, this type of study has shown that blood flow problems in the extracranial portions of the carotid arteries are important in the etiology of cranial neuropathy, including stroke. The external carotid artery, of which the lingual artery is the second branch, is involved in several ways in the pathophysiology and treatment of these conditions. Most notably, the external carotid artery has been shown to (1) maintain cerebral circulation in patients with total occlusion of the extracranial internal carotid, l (2) produce thromboembolic events causing disease in the brain,2 and (3) provide flow for ischemic brain areas via microsurgical bypass procedures.3-5 In its own right, the lingual artery has been used for several years in bypass procedures to supply blood to the basilar artery territory. 6, 7 Furthermore, by virtue of its proximity to the heart and because of characteristics of the entire external carotid artery, the lingual artery theoretically should have a distinctive velocity pulse curve form,H which would be expected to be altered in atherosclerotic disease.g, I4 It is the purpose of this study to identify the velocity pulse curve of the lingual artery in normal, healthy persons and compare it with that found in stroke patients. A previous study indicates that the lingual artery shows atherosclerotic changes in 92 percent of a group examined, including a subject less 252
Fig. 1. Artist’s rendering of human lingual artery including its source and terminal branches. A, Frontal view. B, Sagittal view. 0030-4220/81/030252+04$00.40/0
0
1981 The C. V. Mosby Co.
Lingual artery hemodynamicsin stroke patients 253
Volume 51 Number 3
Fig. 2. Demonstration of clinical use of Doppler flowmeter, including probe placement. than 1 year old. lo It is hoped that eventually the course of atherosclerosis with aging can be determined noninvasively and that this study can provide a piece of information toward that goal. MATERIALS AND METHODS Dissection Prior to this investigation, a dissection of a cadaver’s tongue was carried out to determine the course of the lingual artery intraorally. The deep lingual and sublingual arteries were exposed, and the deep lingual artery was chosen for study because of its easier access and lack of anastomosis with the facial artery (Fig. 1). Subjects Twenty-two healthy volunteers (with no cardiovascular and other diseases and on no medication), aged 17 through 28, were used in our normal group. The stroke group consisted of seven patients of the New York University Institute of Rehabilitation Medicine, all of whom carried a diagnosis of completed cerebrovascular accidents in the carotid artery territory. These patients were taking a variety of medications, primarily antiarrhythmia and antihypertensive drugs. All were essentially normotensive when studied. Equipment A directional Doppler Model 806 ultrasonic flowmeter (Park Electronics, Beaverton, Ore.) was used for qualitative determination of velocity pulse (Fig. 2). This was connected to a Grass polygraph for printed readouts. Stereophonic headphones were used by the investigator to localize the artery and to separate venous from arterial flow.
Fig. 3. Polygraph recording of the velocity pulse of the deep lingual artery of three young, healthy adults.
Procedure Prior to investigation, all subjects’ deep lingual arteries were palpated. Then the subjects were instructed to open their mouths and lift their tongues to the palatal aspect of the maxillary central incisors. The probe was held at approximately a 45degree angle to the arteries. Readings on normal subjects were repeated on separate days to ensure reproducibility of results. Both left and right lingual arteries were examined for approximately lo-second intervals until the investigator believed, on the basis of audio-output, flowmeter, and polygraph recordings, that a maximum velocity had been obtained. Pulse rate and rhythm were determined by examination of the pulse curves. All subjects and patients were seated throughout the studies.
254
Myers, Davis,
and Barker
Oral Surg. March. 1981
Fig. 4. The sametype of recording as shown in Fig. 3 in two stroke patients. Table 1. Velocity pulse wave form descriptors of the deep lingual artery Patient no.
Dicroric notches
Multiple sysrolic und diastolic peaks
Diusrolic
+
+
>2 mm.
Regular
I/I
-
-
0
Regular Regular Irregular Irregular Regular
3/5 3/5 l/l l/l 5/S
POW
Pulse rhythm
Pulse duration Time between systoles
Normal (control) group All patients
Stroke group I 2 3 4 5 6 I
f -
+ = presence of notches and peaks. - = Absence of notches and peaks. Millimeter readings refer to lines on recording
+ Anomalous Anomalous
0 3 mm. 5 mm. 0
flow patterns flow patterns
paper and have no absolute
RESULTS Controls Young healthy persons showed a characteristic, reproducible velocity pulse form in their lingual arteries (Fig. 3). This form includes a sharp systolic peak and a prominent dicrotic notch. Other notable features include multiple systolic and diastolic peaks and good diastolic (base line) flow. The pulses were bilaterally symmetrical in magnitude and form, and heart rate and rhythm were shown to be normal. The readings were all clear and showed no evidence of venous interference. One subject had to be eliminated from the study because of apparent subluxation of the mandible during the test. Another subject was not included in the study because readings showed erratic curves and rhythms. Subsequent electrocardiograph readings showed normal cardiac function, indicating that there was probably anomalous anatomy in the lingual vasculature. Values for all parameters measured are found in Table I.
quantitative
value.
Stroke patients Velocity pulse curves of stroke patients showed considerable qualitative differences from those of the controls. These include (1) amorphous flow patterns, (2) diminution or absence of dicrotic notch and accessory peaks, (3) low or absent diastolic flow, and (4) disturbed rhythm. In each patient, bilateral symmetry was observed. One patient demonstrated normal pulse wave forms, and the only evidence of pathosis was an arrhythmia (Fig. 4). Table I compares qualitative velocity pulse descriptors of stroke patients with those of normal subjects. Two patients showed very low flow with anomalous flow patterns which do not fit in with the pulse wave descriptors (Fig. 5). DISCUSSION From this pilot study, we would be inclined to suspect that lingual artery flow is qualitatively and in some
Volume 51 Number 3
Lingual artery hemodynamicsin stroke patients 255 change of nutrients and wastes, as well as indicating the possibility of generalized arteriosclerosis. Future studies will examine quantitative and qualitative flow changes in external carotid artery branches in health, age, and disease. Thz ultimate aim of these studies is.to aid in diagnostic screening, pre- and postoperative monitoring, and following of patients with carotid artery disease. Included in this category are not only atherosclerotic problems but vascular pain syndromes, such as migraine, cluster headache, and, of special interest, the burning tongue syndrome.
Fig. 5. Comparison of velocity pulse curves in deep lingual arteries of normal and stroke patients. Notice especially the deep dichrotic notch in the normal curve and its virtual absence in the stroke patient’s, Notice also the “flat area” between pulses in the stroke curve. This is represented by the pulse duration in Table I (stroke low diastolic flow and Interval betweenpulses Patient I).
deranged in stroke patients. The quantitative derangements (extremely slow flow) are either the result of occlusive vascular disease In the deep lingual artery or proximal to it, to vasoconstriction, or to a decreased inotropic effect of the heart. The significance of the qualitative changes is as follows: (I) Totally amorphous flqw patterns were found in the two patients exhibiting very low Rows. Several studies indicate that physiologic pulsatiel flow maintains organs at a higher functional level than nonpuisatile flow.‘** I2 *he changes in flow patterns are probably due to arterial occlusion and decreased vessel elasticity. (2) Great diminution or absence of the dicrotic notch and accessory notches was found in all but one stroke patient. The dicrotic notch is caused by a period of reverse flow corresponding to negative pressure due to the closing of the aortic valve. The proximal branches of the external carotid artery are uniquely sensitive to this flow change. In subjects with an elastic arterial system, these notches are transmitted along the arterial tree and are damped our distally. In sclerotic arteries, however, these notches are damped out more quickly.12 (3) Very low or absent diastolic flow is another sequel to decreased arterial elasticity.s This is responsible for limiting the time during which bloodtissue interactions can occur. (4) Disturbed cardiac rhythm likewise would tend to interfere with tissue excases quantitatively
REFERENCES
1. Clayson, K. R., et al.: Importanceof the External Carotid Artery in Extracranial Cerebrovascular Disease, South. Med. J. 70: 904-909, 1977. . 2. Karmody, A. M., Shah, D. M., Monaco, V. J., and Leathep, R. P.: On Surgical Reconstructionof the External Carotid Artery, Am. J. Surg. 136: 177, 1978. 3. Holbach, K. H., Wassmann, H., Bodos, M., and Bonatelli, A. P.: Superficial Temporal Middle Cerebral Artery Anastomosis for Internal Carotid Occlusion, Acta Neurochir. 37: 201-217, 1977. 4. Popp, A. J., and Chater, N.: Extracranial-to-Intracranial Vascular Anastomosis, Surgery 82: 648, 1977. 5. McDowell, F.: The Extracranial-Intracranial Bypass Study, Stroke 8: ‘545, 1977. 6. Whang, C. J., Mozingo, J. R., and Rhoton, A. L., Jr.: Comparison of Blood Flow and Patency in Arterial and Vein Grafts to Basilar Artery, Stroke 6: 445-448, 1975. 7. Khodadad, G.: Sublingual and Lingual-Basilar Artery Anastomoses and Carotid Basilar Bypass Grafts, Surg. Neural. 1: 175-177, 1973. 8. Davson, H., and Segal, M. B.: Introduction to Physiology, New York, 1975, Grune & Stratton, vol. I, p. 260. 9. Lee, B. K., and Trainor, F. S.: Peripheral Vascular Surgery, New York, 1973, Appleton-Century-Crofts, p. 26. 10. Driezen, S., Levy, B., Stem, M., and Bemick, S.: Human Lingual Atherosclerosis, Arch. Oral Biol. 19: 813, 1974. 11. Lee, B. K., and Trainor, F. S.: Peripheral Vascular Surgery, New York, 1973, Appleton-Century-Crofts, chap. 1. 12. Keller, H., Meier, W., Yonekawa, Y., and Kumpe, D.: Noninvasive angiography for the Diagnosis of Carotid Artery Disease, Stroke 7: 354, 1976. 13. Hellekant, G.: Circulation of the Tongue, Oral Physiology, Oxford, 1972, PergammonPress, p. 127. 14. Sofferman, R. A.: Lingual Infarction in Cranial Arteritis, J.A.M.A. 243: 2422, 1980. Reprint
requests to:
Dr. Daniel Myers Department of Oral Medicine SUNYAB Dental School Buffalo, N. Y. 14214
E. Myers, D.D.S., YORK
UNIVERSITY
Sanders Davis,
INSTITUTE
M.D.,
OF REHABILITATION
and June N. Barker,
Ph.D.,
New York, N, Y,
MEDICINE
Doppler blood flow studies were carried out on deep lingual arteries of young adults and stroke patients to see how the hemodynamics of this artery would be altered in the stroke group, who were selected on the basis of their having carotid atherosclerosis. The healthy controls exhibited a consistent and characteristic velocity pulse profile, which included a distinctive dichrotic notch and significant diastolic flow. The stroke group especially lacked these two critical parameters, and some exhibited amorphous flow patterns and cardiac arrhythmias. Implications of these findings in relationship to atherosclerosis are discussed.
W
ith the advent of inexpensive, accurate, and noninvasive methods for clinical blood flow studies, the role of hemodynamic disturbances in systemic disease processes can be investigated. Of particular interest, this type of study has shown that blood flow problems in the extracranial portions of the carotid arteries are important in the etiology of cranial neuropathy, including stroke. The external carotid artery, of which the lingual artery is the second branch, is involved in several ways in the pathophysiology and treatment of these conditions. Most notably, the external carotid artery has been shown to (1) maintain cerebral circulation in patients with total occlusion of the extracranial internal carotid, l (2) produce thromboembolic events causing disease in the brain,2 and (3) provide flow for ischemic brain areas via microsurgical bypass procedures.3-5 In its own right, the lingual artery has been used for several years in bypass procedures to supply blood to the basilar artery territory. 6, 7 Furthermore, by virtue of its proximity to the heart and because of characteristics of the entire external carotid artery, the lingual artery theoretically should have a distinctive velocity pulse curve form,H which would be expected to be altered in atherosclerotic disease.g, I4 It is the purpose of this study to identify the velocity pulse curve of the lingual artery in normal, healthy persons and compare it with that found in stroke patients. A previous study indicates that the lingual artery shows atherosclerotic changes in 92 percent of a group examined, including a subject less 252
Fig. 1. Artist’s rendering of human lingual artery including its source and terminal branches. A, Frontal view. B, Sagittal view. 0030-4220/81/030252+04$00.40/0
0
1981 The C. V. Mosby Co.
Lingual artery hemodynamicsin stroke patients 253
Volume 51 Number 3
Fig. 2. Demonstration of clinical use of Doppler flowmeter, including probe placement. than 1 year old. lo It is hoped that eventually the course of atherosclerosis with aging can be determined noninvasively and that this study can provide a piece of information toward that goal. MATERIALS AND METHODS Dissection Prior to this investigation, a dissection of a cadaver’s tongue was carried out to determine the course of the lingual artery intraorally. The deep lingual and sublingual arteries were exposed, and the deep lingual artery was chosen for study because of its easier access and lack of anastomosis with the facial artery (Fig. 1). Subjects Twenty-two healthy volunteers (with no cardiovascular and other diseases and on no medication), aged 17 through 28, were used in our normal group. The stroke group consisted of seven patients of the New York University Institute of Rehabilitation Medicine, all of whom carried a diagnosis of completed cerebrovascular accidents in the carotid artery territory. These patients were taking a variety of medications, primarily antiarrhythmia and antihypertensive drugs. All were essentially normotensive when studied. Equipment A directional Doppler Model 806 ultrasonic flowmeter (Park Electronics, Beaverton, Ore.) was used for qualitative determination of velocity pulse (Fig. 2). This was connected to a Grass polygraph for printed readouts. Stereophonic headphones were used by the investigator to localize the artery and to separate venous from arterial flow.
Fig. 3. Polygraph recording of the velocity pulse of the deep lingual artery of three young, healthy adults.
Procedure Prior to investigation, all subjects’ deep lingual arteries were palpated. Then the subjects were instructed to open their mouths and lift their tongues to the palatal aspect of the maxillary central incisors. The probe was held at approximately a 45degree angle to the arteries. Readings on normal subjects were repeated on separate days to ensure reproducibility of results. Both left and right lingual arteries were examined for approximately lo-second intervals until the investigator believed, on the basis of audio-output, flowmeter, and polygraph recordings, that a maximum velocity had been obtained. Pulse rate and rhythm were determined by examination of the pulse curves. All subjects and patients were seated throughout the studies.
254
Myers, Davis,
and Barker
Oral Surg. March. 1981
Fig. 4. The sametype of recording as shown in Fig. 3 in two stroke patients. Table 1. Velocity pulse wave form descriptors of the deep lingual artery Patient no.
Dicroric notches
Multiple sysrolic und diastolic peaks
Diusrolic
+
+
>2 mm.
Regular
I/I
-
-
0
Regular Regular Irregular Irregular Regular
3/5 3/5 l/l l/l 5/S
POW
Pulse rhythm
Pulse duration Time between systoles
Normal (control) group All patients
Stroke group I 2 3 4 5 6 I
f -
+ = presence of notches and peaks. - = Absence of notches and peaks. Millimeter readings refer to lines on recording
+ Anomalous Anomalous
0 3 mm. 5 mm. 0
flow patterns flow patterns
paper and have no absolute
RESULTS Controls Young healthy persons showed a characteristic, reproducible velocity pulse form in their lingual arteries (Fig. 3). This form includes a sharp systolic peak and a prominent dicrotic notch. Other notable features include multiple systolic and diastolic peaks and good diastolic (base line) flow. The pulses were bilaterally symmetrical in magnitude and form, and heart rate and rhythm were shown to be normal. The readings were all clear and showed no evidence of venous interference. One subject had to be eliminated from the study because of apparent subluxation of the mandible during the test. Another subject was not included in the study because readings showed erratic curves and rhythms. Subsequent electrocardiograph readings showed normal cardiac function, indicating that there was probably anomalous anatomy in the lingual vasculature. Values for all parameters measured are found in Table I.
quantitative
value.
Stroke patients Velocity pulse curves of stroke patients showed considerable qualitative differences from those of the controls. These include (1) amorphous flow patterns, (2) diminution or absence of dicrotic notch and accessory peaks, (3) low or absent diastolic flow, and (4) disturbed rhythm. In each patient, bilateral symmetry was observed. One patient demonstrated normal pulse wave forms, and the only evidence of pathosis was an arrhythmia (Fig. 4). Table I compares qualitative velocity pulse descriptors of stroke patients with those of normal subjects. Two patients showed very low flow with anomalous flow patterns which do not fit in with the pulse wave descriptors (Fig. 5). DISCUSSION From this pilot study, we would be inclined to suspect that lingual artery flow is qualitatively and in some
Volume 51 Number 3
Lingual artery hemodynamicsin stroke patients 255 change of nutrients and wastes, as well as indicating the possibility of generalized arteriosclerosis. Future studies will examine quantitative and qualitative flow changes in external carotid artery branches in health, age, and disease. Thz ultimate aim of these studies is.to aid in diagnostic screening, pre- and postoperative monitoring, and following of patients with carotid artery disease. Included in this category are not only atherosclerotic problems but vascular pain syndromes, such as migraine, cluster headache, and, of special interest, the burning tongue syndrome.
Fig. 5. Comparison of velocity pulse curves in deep lingual arteries of normal and stroke patients. Notice especially the deep dichrotic notch in the normal curve and its virtual absence in the stroke patient’s, Notice also the “flat area” between pulses in the stroke curve. This is represented by the pulse duration in Table I (stroke low diastolic flow and Interval betweenpulses Patient I).
deranged in stroke patients. The quantitative derangements (extremely slow flow) are either the result of occlusive vascular disease In the deep lingual artery or proximal to it, to vasoconstriction, or to a decreased inotropic effect of the heart. The significance of the qualitative changes is as follows: (I) Totally amorphous flqw patterns were found in the two patients exhibiting very low Rows. Several studies indicate that physiologic pulsatiel flow maintains organs at a higher functional level than nonpuisatile flow.‘** I2 *he changes in flow patterns are probably due to arterial occlusion and decreased vessel elasticity. (2) Great diminution or absence of the dicrotic notch and accessory notches was found in all but one stroke patient. The dicrotic notch is caused by a period of reverse flow corresponding to negative pressure due to the closing of the aortic valve. The proximal branches of the external carotid artery are uniquely sensitive to this flow change. In subjects with an elastic arterial system, these notches are transmitted along the arterial tree and are damped our distally. In sclerotic arteries, however, these notches are damped out more quickly.12 (3) Very low or absent diastolic flow is another sequel to decreased arterial elasticity.s This is responsible for limiting the time during which bloodtissue interactions can occur. (4) Disturbed cardiac rhythm likewise would tend to interfere with tissue excases quantitatively
REFERENCES
1. Clayson, K. R., et al.: Importanceof the External Carotid Artery in Extracranial Cerebrovascular Disease, South. Med. J. 70: 904-909, 1977. . 2. Karmody, A. M., Shah, D. M., Monaco, V. J., and Leathep, R. P.: On Surgical Reconstructionof the External Carotid Artery, Am. J. Surg. 136: 177, 1978. 3. Holbach, K. H., Wassmann, H., Bodos, M., and Bonatelli, A. P.: Superficial Temporal Middle Cerebral Artery Anastomosis for Internal Carotid Occlusion, Acta Neurochir. 37: 201-217, 1977. 4. Popp, A. J., and Chater, N.: Extracranial-to-Intracranial Vascular Anastomosis, Surgery 82: 648, 1977. 5. McDowell, F.: The Extracranial-Intracranial Bypass Study, Stroke 8: ‘545, 1977. 6. Whang, C. J., Mozingo, J. R., and Rhoton, A. L., Jr.: Comparison of Blood Flow and Patency in Arterial and Vein Grafts to Basilar Artery, Stroke 6: 445-448, 1975. 7. Khodadad, G.: Sublingual and Lingual-Basilar Artery Anastomoses and Carotid Basilar Bypass Grafts, Surg. Neural. 1: 175-177, 1973. 8. Davson, H., and Segal, M. B.: Introduction to Physiology, New York, 1975, Grune & Stratton, vol. I, p. 260. 9. Lee, B. K., and Trainor, F. S.: Peripheral Vascular Surgery, New York, 1973, Appleton-Century-Crofts, p. 26. 10. Driezen, S., Levy, B., Stem, M., and Bemick, S.: Human Lingual Atherosclerosis, Arch. Oral Biol. 19: 813, 1974. 11. Lee, B. K., and Trainor, F. S.: Peripheral Vascular Surgery, New York, 1973, Appleton-Century-Crofts, chap. 1. 12. Keller, H., Meier, W., Yonekawa, Y., and Kumpe, D.: Noninvasive angiography for the Diagnosis of Carotid Artery Disease, Stroke 7: 354, 1976. 13. Hellekant, G.: Circulation of the Tongue, Oral Physiology, Oxford, 1972, PergammonPress, p. 127. 14. Sofferman, R. A.: Lingual Infarction in Cranial Arteritis, J.A.M.A. 243: 2422, 1980. Reprint
requests to:
Dr. Daniel Myers Department of Oral Medicine SUNYAB Dental School Buffalo, N. Y. 14214