Assessment of a Newly Recognized Association
Carotid Sinus Hypersensitivity and Denervation of Sternocleidomastoid Muscles
Background Carotid sinus syndrome has been reported recently to be associated with chronic denervation of the sternocleidomastoid muscles. To further understand the relationship between carotid mechanoreceptors and sternocleidomastoid denervation, the present study investigated the relation between the results of carotid sinus massage and electromyographic activity of the sternocleidomastoid muscles in patients without syncope.
Methods and Results Patients were selected prospectively if they fulfilled strict exclusion criteria, particularly the absence of a history of syncope, pacemaker implantation, or drugs known to modify the behavior of the autonomic nervous system. A right and left carotid massage was performed for 10 seconds in 30 patients (22 men; mean age, 67.3±6.5 years). The results (monitoring for heart rate and blood pressure) were classified as normal, doubtful, or hypersensitive carotid sinus. Sternocleidomastoid electromyography activity was recorded from the right and left sides, and the results were classified as normal, moderate denervation, and severe denervation. Carotid sinus massage was normal in 13 patients (43%), doubtful in 9 (30%), and abnormal in 8 (27%). Electromyographic activity of the sternocleidomastoids was normal in 13 patients (43%) and revealed moderate denervation in 7 (24%) and severe chronic denervation in 10 (33%). The results of carotid sinus massage and sternocleidomastoid electromyography were highly concordant in each patient (κ=.592, P<.00001) and in each side (right, κ=.381, P<.03; left, κ=.390, P<.01).
Conclusions Carotid sinus hypersensitivity and chronic denervation is a common finding in individuals older than 50 years of age. These two entities are significantly related, suggesting a pathophysiological relation of one to the other.
Carotid sinus syndrome is a well-established cause of syncope1 usually treated by pacemaker implantation.2 3 4 5 Although the pathophysiology of this syndrome remains incompletely understood, interest in carotid sinus syndrome has been rekindled by the evidence of an association between carotid sinus syndrome and peripheral denervation of the sternocleidomastoid muscles. Although the reasons for this association remain speculative, the hypothesis was that denervation of the sternocleidomastoid muscles probably is associated with a defect of proprioceptive information flow. The central nervous system, without any information about the contractile state of the muscles, interprets any information coming from the carotid sinus receptors only as an abrupt increase in blood pressure and reacts by a dramatic decrease in heart rate and/or blood pressure.6 The present study was undertaken to determine (1) the prevalence of asymptomatic carotid sinus hypersensitivity in patients admitted in a cardiology department, (2) the prevalence of sternocleidomastoid muscle denervation in the same population, and most importantly, (3) the concordance between these two findings.
The study group was recruited prospectively from patients admitted in the cardiology department and who were older than 50 years of age and in sinus rhythm. Patients were excluded if they met any of the following criteria: (1) history of previous syncope or severe dizziness, (2) pacemaker implantation, (3) treatment by β-blockers or digitalis (or discontinued for more than five half-lives), (4) previous surgery of the neck or known disease of the cervical region, (5) carotid bruit, (6) recent myocardial infarction, cardiac surgery (<3 months), or more generally acute disease (cardiac failure, fever), (7) diabetes, (8) excessive alcohol consumption, (9) peripheral or central neurological disease, and (10) absence of informed consent to undergo the following noninvasive procedure.
Carotid Sinus Massage
Carotid sinus massage was performed in all patients by the same physician (J.-J.B.) in a quiet room (usually devoted to head-up tilt test). The patient was supine and continuously monitored for heart rate and noninvasively7 for blood pressure (Finapres Ohmeda). The patient was left quiet for 5 minutes to allow stabilization of heart rate and blood pressure. Recordings were performed 10 seconds before the beginning of the massage and ended when the parameters returned to their baseline values. The right carotid artery was first massaged longitudinally for a duration of 10 seconds; after 5 minutes of rest, the left artery was massaged for the same duration. The procedure was repeated once, and the results were analyzed for each patient separately for each side and correlated with the electromyographic recordings from the same side. In case of discordance between the two massages in a single patient or in a single side, the more “abnormal” was retained and interpreted according to the classification reported in Table 1⇓. For each patient and for each side, the result was expressed as normal, doubtful, or definite carotid sinus hypersensitivity (criteria provided are defined in Table 1⇓).
On the same day as the carotid sinus massage was performed, the patient was evaluated in the neurophysiological laboratory. Electromyography was registered in all patients by the same physician (G.L.), who was unaware of the results of the carotid sinus massage. Electromyographic activity of the right and left sternocleidomastoids was recorded by concentric needle electrode with a recording area of 0.07 mm.
The subject was in supine position. The needle electrode was inserted into the sternocleidomastoid at the level of the cricoid cartilage, the head being in a medium position. The subject was asked to rotate the head on the opposite side, slightly flexed, and to resist to an opposite strength. Examination was performed at 10 sites for each muscle; electromyographic activity (Nicolet Vicking II) was recorded between a bandpass of 20 Hz and 10 kHz. A classic analysis was performed of spontaneous activity at rest and the motor unit potential morphology and recruitment during an increasing volitional activity. According to the volitional electromyographic activity, each sternocleidomastoid was characterized as normal activity (interferential pattern, normal motor unit potentials), moderate denervation (rich tracings, including excessive polyphasic motor unit potentials or abnormal recruitment), or severe denervation (poor electromyographic activity with excessive polyphasic motor unit potentials and recruitment abnormalities) (Figure⇓).
Data are expressed as mean=SEM. Comparisons between categorical data were made with the χ2 test with Yates' correction. The κ test was used to analyze the concordance between the carotid sinus massage and the electromyographic results; its significance was evaluated by normal approximation for large samples.8 Statistical significance was presumed for a value of P<.05.
During a 3-month period, 34 patients fulfilled the inclusion and exclusion criteria; 4 of these individuals were excluded for unsuitable blood pressure recordings (1 patient with Raynaud phenomenon and 2 with very thin fingers) or electromyographic recordings (1 patient who refused to cooperate during the procedure). Consequently, the study group consisted of 30 patients (22 men and 8 women; mean age, 67.3±6.5 years).
Results by Patient
Investigations were completed without any complication. Carotid sinus massage resulted in a normal response (IA-IIA, according to Table 1⇑) in 13 patients (43%); in the remaining 17 patients (57%), the result was either doubtful (9 patients [30%]) or in favor of a definite carotid sinus hypersensitivity (8 patients [27%]). Table 2⇓ gives the precise classification for these 17 patients. In the 8 patients with obvious carotid sinus hypersensitivity, the vasodepressor response (IIC) was more frequent (6 patients) than the cardioinhibitory one (IC) (3 patients; 1 had both responses).
Electromyographic investigation of the sternocleidomastoids revealed abnormal tracings in 17 patients (57%); chronic denervation (no case of acute denervation) was considered moderate in 7 (24%) and severe in 10 (33%). The signs of denervation were bilateral in 10 patients and unilateral in 7.
The concordance between normal carotid sinus massage and normal sternocleidomastoid muscles was excellent (85%), as was the concordance between an abnormal carotid sinus massage and signs of severe denervation of at least one of the sternocleidomastoid muscles (75%, Table 3⇓). Altogether, the concordance between the two parameters according to the κ test (κ=.592) was highly significant (P<.00001).
Results by Sides
The concordance between a normal right carotid sinus massage and absence of denervation of the right sternocleidomastoid muscle was found in 83% of the patients and the reverse in 71% (if moderate abnormal results of electromyography were included the proportion, it was increased to 87.5%). These results (Table 4⇓) are statistically significant (κ=.381, P<.03). In case of left carotid sinus massage (Table 4⇓), the proportions were identical and remained statistically significant (κ=.390, P<.01).
Abnormal Electromyographic Results and Doubtful Carotid Sinus Massage
As indicated in Tables 3⇑ and 4⇑, moderate or definite signs of chronic denervation of the right sternocleidomastoid muscle were frequently associated with doubtful responses to carotid sinus massage (8 of 9 for the patients as a whole, 3 of 5 for the right side, and 10 of 11 from the left). However, the association of normal electromyographic activity with a doubtful response to carotid sinus massage was significantly less frequent: 1 of 9 for the patients (P<.05), 2 of 5 for the right side (NS), and 1 of 11 for the left side (P<.02).
The principal finding in this study was the large proportion of individuals without syncope or dizziness who exhibited both hypersensitive carotid sinus and chronic denervation of the ipsilateral sternocleidomastoid muscle.
Carotid Sinus Hypersensitivity
The difference between carotid sinus syndrome and carotid sinus hypersensitivity is the lack of spontaneous symptoms in the latter situation.9 This absence of symptoms probably explains why the pathophysiology of carotid sinus hypersensitivity is poorly known. In our cohort of 30 asymptomatic patients, more than one quarter exhibited clear-cut overt carotid sinus hypersensitivity, mainly the vasodepressor form, a result in agreement with other series.10 11 12 13 The natural history of this finding in these patients is unknown: Will they remain asymptomatic or experience syncope? Only a careful prospective follow-up of a large number of such individuals will provide an answer to this question. The classification of the patients considered to have doubtful or intermediate response (defined as class B in our nomenclature; see Table 1⇑) is also unknown: Is this response within normal limits or an attenuated abnormal one? This point will be discussed, but again a prospective follow-up is necessary to definitely answer this question.
Denervation of the Sternocleidomastoid Muscles
In a previous report, we found that 23% of the control patients had chronic denervation of the sternocleidomastoid muscles. However, only patients without carotid sinus hypersensitivity were included.6 This factor could explain the reason why the proportion is much higher in the present series, with 57% of patients having moderate or severe signs of chronic denervation.
Association Between Carotid Hypersensitivity and Denervation of Sternocleidomastoid Muscles
Chronic denervation of the sternocleidomastoid muscles has been reported in patients with carotid sinus syndrome.6 The present study reinforces the concept of a relation between an abnormal response to carotid sinus massage and denervation of the sternocleidomastoid muscles in patients without syncope but who exhibit carotid sinus hypersensitivity. Furthermore, these abnormalities are significantly associated even if only one side is considered. This finding is a strong argument to assume that one of these processes is a direct consequence of the other.
Another important finding is that the relation between the so-called doubtful response to carotid sinus massage and denervation of the sternocleidomastoid muscles is as frequent as in clear-cut abnormal carotid sinus massage response. Possibly, this observation may indicate that these “doubtful” responses are indeed abnormal. If we consider this hypothesis, then Tables 3⇑ and 4⇑ can be simplified: The carotid sinus massage is either normal or abnormal, and so are the electromyographic results (which is the case, as “EMG ±” does not mean doubtful but moderately abnormal). The “new” results are summarized in Table 5⇓, and this presentation enhances the proposed relationship between carotid hypersensitivity and electromyographic findings and vice versa.
The hypothesis that we have formulated to explain the relationship between denervation and abnormal response to carotid sinus massage has been extensively described6 and is based on the theory of central gating.14 Briefly, chronic denervation of the muscle leaves the central nervous system without any moment-to-moment information about the contractile state of the muscle. On the other hand, the midbrain centers receive “normal” information from the stretch receptors of the carotid sinus. In a normal individual, carotid sinus massage, because of the anatomic position of the sternocleidomastoid muscle, results in a pressure on both the muscle and the sinus, and these signals are integrated by the centers as an “external” stretching of the sinus. In the case of proprioceptive defect of the muscle, the massage of the sinus is considered as a stretching of the sinus only and is integrated by the centers as an abrupt increase in blood pressure, resulting through the baroreflex pathways in an inappropriate and dramatic decrease in heart rate and/or systolic blood pressure due to a potent vasodilatation.
Although concordance between results of carotid sinus massage and electromyographic tracings of the sternocleidomastoids is statistically highly significant, there are a few conflicting findings, ie, a normal carotid massage in the case of pathological electromyography or the reverse. In the former situation, the relative lack of reproducibility of carotid sinus massage could be indicated; in the latter, we may assume that the muscle is not uniformly damaged and that the diseased area has not been explored, the last hypothesis being a heterogeneity of pathophysiology of carotid sinus hypersensitivity.
Limitations of the Study
The main results of this study are based on physicians' observations and particularly the electromyographic findings. However, the interobserver and intraobserver reproducibilities in this case have been reported to be excellent.15
Although this study shows an association between carotid sinus hypersensitivity and denervation of sternocleidomastoid muscles, it does not demonstrate a clear relationship between these two entities. Furthermore, it raises many questions: Is this denervation age related (our study group was older than 50 years), or does it exist also in younger people? Does this proportion represent the prevalence in the general population or has it been biased by the recruitment in a cardiology department? What is the cause of denervation? Is it just a physiological process, or does it carry pathological consequences?
Carotid sinus hypersensitivity is a frequent finding in individuals older than 50 years. Chronic denervation of the sternocleidomastoid muscles is common in this population and probably induces the abnormal response to carotid sinus massage. This observation leads us to consider that the sternocleidomastoid muscle could be a contributor to cardiovascular regulation.
- Received August 6, 1996.
- Revision received December 5, 1996.
- Accepted December 16, 1996.
- Copyright © 1997 by American Heart Association
Roskam J. Un syndrome nouveau: syncopes cardiaques graves et syncopes répétées par hypereflexivité sinocarotidienne. Presse Med. 1930;38:590-591.
Morley CA, Perrins EJ, Grant P, Chan SL, McBrien DJ, Sutton R. Carotid sinus syncope treated by pacing: analysis of persistent symptoms and role of atrioventricular sequential pacing. Br Heart J. 1982;47:411-418.
Brignole M, Menozzi C, Lolli G, Bottoni N, Gagglioni G. Long-term outcome of paced and non paced patients with severe carotid sinus syndrome. Am J Cardiol. 1992;69:1039-1043.
Tea SH, Mansourati J, L'Hévéder G, Mabin D, Blanc JJ. New insights in the pathophysiology of carotid sinus syndrome. Circulation. 1996;93:1411-1416.
Imholz BPM, Settels JJ, Van der Meiracker AH, Wesseling KH, Wieling W. Non-invasive continuous blood pressure measurement during orthostatic stress compared to intra-arterial pressure. Cardiovasc Res. 1990;24:214-221.
Almquist A, Gornick C, Benson W, Dunningan A, Benditt DG. Carotid sinus hypersensitivity: evaluation of the vasodepressor component. Circulation. 1985;71:927-936.
McIntosh S, Lawson J, Kenny RA. Clinical characteristics of vasodepressor cardio inhibitory and mixed carotid sinus syndrome in the elderly. Am J Med. 1993;85:203-208.