Quantitative Analysis of the Oculocardiac by Traction on Human Extraocular Muscle

Tsutomu Ohashi, Manabu Kase, and Masahiko Yokoi

The was quantitatively studied in 15 patients with strabismus. The reflex was observed in all patients when the medial rectus and inferior oblique muscles were stretched; the medial rectus muscle had a lower threshold than the inferior oblique. was evoked in 7 of the 15 patients when the lateral rectus was tractioned with tensions of 50 g and 600 g. The oculocardiac reflex was a graded phenomenon as a function of tension applied to the extraocular muscles. As tension was increased, bradycardia occurred rapidly and became deep. Systemic administration of prevented completely the bradycardia from occurring. The results suggest that the response of the extraocular muscles to stretch are critically mediated through a polysynaptic path to the , resulting in suppression of the . Invest Ophthalmol Vis Sci 27:1160-1164, 1986

The oculocardiac reflex is a physiological response Materials and Methods of the heart to physical stimulation of the eye or the The oculocardiac reflex was examined in 15 patients ocular adnexa, characterized by bradycardia or ar- with strabismus under general anesthesia. Their ages rhythmia, which sometimes leads to cardiac arrest.1 ranged from 11 months-10 yr. Seven of the 15 patients The major pathway mediating the oculocardiac reflex were exotropes, and eight were esotropes with or with- seems to consist of an afferent link through the out overaction of the inferior oblique muscle. None of ophthalmic portion of the to the vagus the patients had cardiac or neurological disorders. The nuclei and an efferent link through the to premedication for general anesthesia was diazepam the heart.2-3 (0.1 mg/Kg). Measurements were taken in all patients It has been shown that the oculocardiac reflex oc- without preoperative administration of atropine, and curred most frequently when the medial rectus was atropine was used later in surgery in four patients. In- stimulated, but the incidence of the reflex with stim- formed consents were signed by all patients and their ulation of the medial rectus has varied among previous parents. reports.4'5 Such results suggest the reflex may differ in The heart rate was recorded from lead II of the elec- different people and for different muscles. trocardiogram (ECG) which was presented as an in- In order to understand the mechanism of the reflex stantaneous frequency by transforming from a QRS and discrepancies on previous data, the relationship spike of the ECG to a of 1 msec duration and between input and output in the reflex should be quan- calculating interspike intervals. The extraocular mus- titatively analyzed. Previous studies, however, have not cles were isolated from surrounding tissues and sutures explored the relationship between oculocardiac reflex were placed in the insertions of the muscles and pulled and tension applied to extraocular muscles. We, there- in a direction opposite the muscle field of action. Step- fore, have studied the oculocardiac reflex quantitatively wise traction on the extraocular muscles was given during strabismic surgery. We measured heart rate as manually. The tension of stretch was measured by a an instantaneous frequency and tension of traction on straingauge (San Ei Sokki Co., Sapporo, Japan) fixed extraocular muscles, and have tried to clarify whether to suturing threads. Signals of instantaneous frequency the depth of the oculocardiac reflex is related to the of heart rate and tension were stored on magnetic tape. strength of tension applied to extraocular muscles. For analysis of the data, these signals were displayed on a polygraph (paper speed, 5 cm/sec). The latency of the oculocardiac reflex was measured from the onset From the Department of Ophthalmology, Hokkaido University, of deflection of the tension curve to the pulse just prior School of Medicine, Sapporo 060, Japan. to the beginning of instantaneous frequency curve, Submitted for publication: December 27, 1984. which declined continuously from the baseline level Reprint requests: Manabu Kase, MD, Department of Ophthal- mology, Hokkaido University, School of Medicine, Sapporo 060, before the tension on the extraocular muscles, because Japan. the frequency was presented as the level of the following

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interspike intervals. The measurements of latency in ! 3 •!;•[; T'j-i the present study, however, had errors larger than 0.5 sec as the maximum rate of heart beats was about 120 beats/min. The depth of the oculocardiac reflex was expressed as decrease ratio; i.e., the percentage of the 105 105 difference between the lowest frequency in oculocardiac reflex and the initial frequency before the traction was 75 75 applied to the initial frequency.

70 350 Results Oculocardiac Reflex to Stretch on Extraocular Muscle The heart rate was very regular under general anes- thesia, ranging from 84 beats/min-123 beats/min. 105 Stretch on the extraocular muscles produced changes 105 in heart rate in the form of bradycardia and arrhythmia 75 (Fig. 1). No was observed. The bradycardia 75

and arrhythmia were consistently observed during pe- 1 70 400 riods of traction on the medial rectus (Fig. 1 A), the inferior oblique (Fig. 1B) and the lateral rectus muscles (Fig. 1C). Arrhythmia, however, occurred during steady traction but not during the trajectories of phasic changes in bradycardia. The analysis of instantaneous

frequency of heart rate revealed that the arrhythmia 120 120 appeared in order to compensate for a bradycardia, |%^v since low and high frequencies of heart rate during 90 steady traction applied on the extraocular muscles 90 tended to appear alternately. The intensity of bradycardia changed with the 1 50 400 strength of tension applied to the extraocular muscles. Fig. 1. Bradycardia of the oculocardiac reflex by traction on medial Heart rate decreased from 107 beats/min to 98 beats/ rectus (A), inferior oblique (B), and lateral rectus (C) in a 6-yr-old min (8.6% in decrease ratio) and to 58 beats/min (45%) exotrope. Upper traces are ECG recordings. Lower ones show in- stantaneous frequency calculated from the ECG. Bars indicate the when the medial rectus muscles were stretched by ten- periods of traction and numbers show grams of tension. Dots denote sions of 70 g and 350 g, respectively (Fig. 1A). The 5 sec. contours of bradycardia observed when the inferior oblique muscles were stretched were very similar to those when traction was applied to medial rectus mus- cles. Heart rate decreased 22.5% and 48% of the initial bradycardia ranged 0.67 sec-2.41 sec, which tended to rate when the inferior oblique muscles were stretched be short with increase of tension. They, however, were by tensions of 170 g and 400 g, respectively (Fig. IB). not analyzed in detail any further because of errors However, when lateral rectus muscles were tractioned larger than 0.5 sec on the measurements. Figure 2 also with 150 g of tension, the heart rate did not alter during shows that, as the tension of traction increased from the period of traction (Fig. 1C). Bradycardia of 18% in 100 g to 450 g, the responses of bradycardia to transient decrease ratio appeared in association with traction on changes of traction became more rapid. The heart rate the lateral rectus muscle with tension increased to decreased gradually, although the tension of 100 g was 400 g. applied stepwisely. A rapid decrease in heart rate, how- The occurrence and depth of bradycardia were re- ever, occurred to strong stimuli. The second QRS spike lated to the tension of stretch on the extraocular mus- of bradycardia showed the lowest frequency when the cles. Figure 2 shows a quantitative analysis of the re- tension of 300 g was applied and the first spike already lationship between bradycardia and tension of stretch reached the minimum rate of the heart rate at the ten- applied to the medial rectus. The tensions of 100 g, sion of 450 g. On the other hand, the trajectories re- 150 g, 300 g, and 450 g induced 18%, 25%, 39%, and covering from the bradycardia after the release of trac- 44%, respectively, indicating that the depth of brady- tion showed exponential curves which were identical, cardia increased with tension applied. The latencies of independent of the strength of tension.

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10 0 r 120 bradycardia occurred in all 11 patients, as well as when U the medial rectus muscles were stretched. The stretch on the inferior oblique muscles with tensions below 90 100 g evoked no changes in heart rate in all the patients. The lowest tension to evoke changes was 128 g, indi- cating that the threshold of the inferior oblique muscles is higher than that of the medial rectus muscles. On the other hand, no bradycardia occurred in 7 of the 15 patients when the lateral rectus was stretched with ten- sions to 600 g, suggesting that the incidence of the ocu- 150 r 120 locardiac reflex with traction of the lateral rectus was low. The bradycardia induced with stretch of the lateral rectus was weak; the maximum decrease ratio was 19%. 90 Figure 3 shows the relationship between the depth of bradycardia and the tensions applied to the medial- rectus (Fig. 3A), the inferior oblique (Fig. 3B), and the lateral rectus (Fig. 3C) in three patients who were ex-

300 r 120 A Co)

90

20-

r 120 450 B Co) r 90 40 -I 20-

Fig. 2. Instantaneous frequency in heart rate during traction on the medial rectus with tensions of 100 g, 150 g, 300 g, and 450 g in a 11-month-old esotrope. Bars indicate the periods of traction and numbers are grams of tensions. Dots denote 2.5 sec. Co) 40 H Relationship Between Depth of Bradycardia and Tension 20- The relationship between the depth of bradycardia and the tension was studied in 15 medial rectus, 11 inferior oblique, and 15 lateral rectus muscles of the 15 patients. The muscles were tractioned with tension 100 200 300 ranging from 50 g-600 g. Bradycardia was observed in TENSION (gram) all 15 patients when the medial rectus muscles were stretched, while, in 4 of 15 patients, no bradycardia Fig. 3. Relationship between depth of bradycardia and tension occurred on traction with tensions less than 100 g. The applied to the medial rectus (A), the inferior oblique (B), and the lateral rectus (C) in three cases. Abscessa means tension and ordinate lowest tension to evoke the bradycardia was 60 g. The denotes decrease ratio of the bradycardia. Case 1 (filled circles) was depth of bradycardia, however, differed in different pa- a 6-yr-old exotrope, Case 2 (filled squares) was a 3-yr-old exotrope, tients. When the inferior oblique was stretched, the and Case 3 (filled triangles) was a 4-yr-old esotrope.

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amined with various tensions. Case 1 (Fig. 3, filled cir- cles) showed deep bradycardia to stretch on each mus- cle, whereas case 2 (Fig. 3, filled triangles) showed weak response of oculocardiac reflex to tensions, indicating that there was an interpersonal variation as well as a 120 difference in depth of oculocardiac reflex among the 90 extraocular muscles.

JU30U0 Effect of Atropine on Occurrence of Bradycardia C 0

The oculocardiac reflex was also examined before and after administration of atropine (0.01 mg/Kg, in- travenous) when the medial rectus was stretched with a tension of 300 g (Fig. 4). When the bradycardia was r 180 deep, a supraventricular premature contraction oc- curred, which had a normal duration. Atropine evoked an increase in heart rate from 108 beats/min to 150 L 120 beats/min. No bradycardia was observed in association with stretch on the medial rectus with a tension of 300 300 g 2 min after administration of atropine. The effect r 0 of atropine on preventing the bradycardia from oc- Fig. 4. Effect of atropine on oculocardiac reflex induced by traction curring for more than 30 min. of medial rectus in same case as Figure 2. A, Recording of ECG before atropine. B, Instantaneous frequency associated with A. C, Tension curve during traction on the muscle. D, Recording of ECG Discussion after administration of atropine. E, Instantaneous frequency asso- ciated with D. F, Tension curve during traction on the muscle. Dots Stretch on extraocular muscles produced changes in denote 2.5 sec. A supraventricular extrasystole (arrow) was observed heart rate such as bradycardia and arrhythmia. Brady- in A and B. cardia with arrhythmia was observed in all patients examined. A striking finding was that the bradycardia was a graded phenomenon as a function of the tension ap- cardia of 10% or greater as a positive response of the plied to the extraocular muscles. In addition to the oculocardiac reflex. depth of bradycardia, the period of time to reach the The present study also showed that there were dif- minimum heart rate also became shortened as the ten- ferences of depth and threshold of the reflex as well as sion increased. These results suggest that the depth and incidence among the medial rectus, the inferior oblique, occurrence of bradycardia in the oculocardiac reflex and the lateral rectus muscles. No bradycardia occurred were closely related to the strength of tension, and that on stretching the medial rectus and the inferior oblique the responses of extraocular muscles to stretch were by tensions less than 60 g and 128 g, respectively, in- quantitatively transmitted to the heart and then sup- dicating that the medial rectus had a lower threshold pressed the heart rate. than the inferior oblique. The traction of the lateral The relationship between depth of bradycardia and rectus even by tension less than 100 g, however, evoked the tension showed that the occurrence of the oculo- bradycardia in two of the eight patients who showed cardiac reflex differed in the medial rectus, the inferior oculocardiac reflex with tensions of 50 g to 600 g, but oblique, and the lateral rectus muscles. Stretch on the their bradycardia was significantly weaker than that of medial rectus and the inferior oblique evoked the reflex the other two muscles. What components of the ocu- in all the patients tested, whereas, in the lateral rectus, locardiac reflex arc do the differences among the medial the reflex could be induced in only about 50% of pa- rectus, the inferior oblique, and the lateral rectus result tients. The incidence of oculocardiac reflex, however, from? The afferent system is responsible for their dif- has been reported to range from 16% to 95%.'-4'5'6'7 It ferences, rather than the efferent system including the seems likely that the difference in incidence between vagus nuclei, since the response patterns were identical previous data and ours resulted mainly from differences among the three muscles; the bradycardia occurred in the technique analysis of measurement in heart rate rapidly and recovered exponentially after release. It has and strength of tension applied. In the present study, been believed that the receptors for the reflex are tri- the reflex was clearly observed even when the decrease geminal nerve terminals, muscle spindles,8'9 or Golgi ratio was 2%, whereas other reports defined a brady- tendon organs.10 However, it seems likely that the tri-

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geminal nerve terminals may be considered as the re- References ceptor, because the threshold of the reflex with 60 g is 1. Sorenson EJ and Gilmore JE: Cardiac arrest during strabismus too high for that of muscle spindles," although phys- surgery. Am J Ophthalmol 41:748, 1956. iological characteristics of trigeminal nerve terminals 2. Aschner B: Ueber einen bisher noch nicht beschriebenen Reflex and Golgi tendon organs in extraocular muscles are vom Auge auf Kreislauf and Atmung: Verschwinden des Radi- still obscure, and because the same bradycardia as the alispuls bei Druck auf das Auge. Wien Klin Wochenschr 21: reflex could be induced by stimulations of eye lids,12 1529, 1908. 13 14 3. Sabena V and Posteli T: Oculocardiac reflex: Electrocardiographic face, and oral cavity. study. Folia Cardiol 2:301, 1941. Arrhythmia was always observed in association with 4. Welhalf WR and Johnson DC: The oculocardiac reflex during bradycardia during the period of steady traction on extraocular muscle surgery. Arch Ophthalmol 73:43, 1965. extraocular muscles. The heart rate in arrhythmia 5. Apt L, Isenberg S, and Gaffney WL: The oculocardiac reflex in showed that the heart contracted soon after the pre- strabismus surgery. Am J Ophthalmol 76:533, 1973. 6. Bosomworth PP, Ziegler CH, and Jacoby J: The oculocardiac ceding low frequency contraction, and a supraventric- reflex in eye muscle surgery. Anesthesiol 19:7, 1958. ular premature contraction occurred when the heart 7. Moonie GT, Rees DL, and Elton D: The oculocardiac reflex rate reached around 60 beats/min. The arrhythmia, during strabismus surgery. Cn Anesthesiol Soc J 11:621, 1964. therefore, may occur in order to compensate for 8. Cooper S and Daniel FM: Muscle spindles in human extrinsic bradycardia. Systemic administration of atropine pre- eye muscles. Brain 72:1, 1949. 9. Inoue T: A study on the muscle spindle in the human ocular vented completely the bradycardia and arrhythmia muscles. Igakukenkyu 28:221, 1958. from occurring. This was in good agreement with pre- 10. Ruskell GL: The incidence and variety of Golgi tendon organs vious reports,4'61516 and suggested that the bradycardia in extraocular muscles of the rhesus monkey. J Neurocytol 8: in the reflex is mediated through the vagus nerve. 639, 1979. 11. Bach-y-Rita P and Ito F: Properties of stretch receptors in cat extraocular muscles. J Physiol 186:633, 1966. Key words: oculocardiac reflex, extraocular muscle, brady- 12. Anderson RL: The blepharocardiac reflex. Arch Ophthalmol 96: cardia, arrhythmia, vagus nerve 1418, 1978. 13. Robindeaux V: Oculocardiac reflex caused by midface disim- paction. Anesthesiol 49:433, 1978. Acknowledgments 14. Thurlow AC: Cardiac dysrhythmias in outpatient dental anes- thesia in children. The effect of prophylactic intravenous atropine. We thank Dr. H. Matsuda, the Department of Ophthal- Anesthesia 27:429, 1972. mology, Hokkaido University School of Medicine, and Dr. 15. Deacock AR and Ocer HF: The prevention of S. Jacobson, Bascom Palmer Eye Institute, University of during ophthalmic surgery. Br J Anesthesiol 34:451, 1962. Miami for their valuable criticism during the preparation of 16. Taylor C, Wilson FM, Roesch R, and Stoelting VK: Prevention this manuscript. of the oculocardiac reflex in children. Anesthesiol 24:646, 1963.

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