Journal of Pediatric Ophthalmology and Strabismus

Evaluation of Hemodynamic Changes in the Ophthalmic Artery With Color Doppler Ultrasonography After Strabismus Surgery

Hüseyin Bayramlar, MD; Yüksel Totan, MD; Osman Çkiç, MD; Kamuran Mahmut Yazicioglu, MD; Erdinç Aydin, MD

Abstract

ABSTRACT

Purpose: To investigate the blood flow changes in ophthalmic artery with color Doppler ultrasonography after strabismus surgery.

Methods: Twenty eyes of 19 patients who underwent recession or resection surgery on two horizontal rectus muscles in 1 eye were examined using color Doppler ultrasonography preoperati vely and 1 week and 1 month postoperatively. Measurements from both eyes of 1 6 age- and sex-matched normal subjects served as control data. The systolic maximum velocity, mean velocity, end-diastolic velocity, pulsati I ity index, and resistance index of the ophthalmic artery were determined. The Mann-Whitney U test was performed for comparison of the control and study group preoperatively for any hemodynamic parameter. Statistical comparison of the preoperative and postoperative measures in the study group was performed with Friedman's two-way analysis of variance.

Results: No difference (P>.05) was observed preoperatively between the study and control groups for any hemodynamic parameter in the ophthalmic artery. Although the ophthalmic artery showed a slight increase in systolic maximum velocity 1 month postoperatively, there were no statistically significant differences (P>.05) in velocities or resistance in the ophthalmic artery at any interval.

Conclusion: Two horizontal rectus muscle operations in a previously unoperated eye do not cause significant hemodynamic changes in the ophthalmic artery. However, further studies are needed to obtain more information about the effect of multiple vertical rectus muscle operations on the blood flow parameters of the ophthalmic artery.

Journal of Pediatric Ophthalmology and Strabismus 2000;37:94-100.

Abstract

ABSTRACT

Purpose: To investigate the blood flow changes in ophthalmic artery with color Doppler ultrasonography after strabismus surgery.

Methods: Twenty eyes of 19 patients who underwent recession or resection surgery on two horizontal rectus muscles in 1 eye were examined using color Doppler ultrasonography preoperati vely and 1 week and 1 month postoperatively. Measurements from both eyes of 1 6 age- and sex-matched normal subjects served as control data. The systolic maximum velocity, mean velocity, end-diastolic velocity, pulsati I ity index, and resistance index of the ophthalmic artery were determined. The Mann-Whitney U test was performed for comparison of the control and study group preoperatively for any hemodynamic parameter. Statistical comparison of the preoperative and postoperative measures in the study group was performed with Friedman's two-way analysis of variance.

Results: No difference (P>.05) was observed preoperatively between the study and control groups for any hemodynamic parameter in the ophthalmic artery. Although the ophthalmic artery showed a slight increase in systolic maximum velocity 1 month postoperatively, there were no statistically significant differences (P>.05) in velocities or resistance in the ophthalmic artery at any interval.

Conclusion: Two horizontal rectus muscle operations in a previously unoperated eye do not cause significant hemodynamic changes in the ophthalmic artery. However, further studies are needed to obtain more information about the effect of multiple vertical rectus muscle operations on the blood flow parameters of the ophthalmic artery.

Journal of Pediatric Ophthalmology and Strabismus 2000;37:94-100.

INTRODUCTION

Color Doppler ultrasonography is a relatively new technology that offers noninvasive, painless imaging of retrobulbar circulation. It is an ultrasound technique that combines die gray-scale Bscan imaging of tissue structure and color-encoded representation of blood flow, providing accurate and reproducible velocity and resistance measurements.

In the past few years, color Doppler ultrasonography has found a number of applications after ophthalmic surgery including scleral buckling, trabeculectomy, and optic nerve decompression.1"4 Regulo et al1 found a significant reduction in blood flow velocities in the central retinal artery but not in the ophthalmic artery after unilateral successful scleral buckling procedures. In contrast, Santos et al2 reported decreased flow velocities in the ophthalmic artery associated with an increase in intraocular pressure (IOP) following buckling surgery compared to die preoperative values in die same eyes. Trible et al3 reported a sustained increase in mean and end-diastolic velocity, and a decrease in resistance index in die central retinal and short posterior arteries with clinically attainable reductions in IOP after trabeculectomy in glaucoma patients. The study results also showed a transient increase in flow velocities in the ophdialmic artery after die procedure. In a study by Mittra et al,4 optic nerve decompression was found to improve die blood flow to die edematous optic nerve head and thus considered to be a contributing factor for visual improvement after the procedure. AH of diese studies commonly demonstrated blood flow changes, significant or insignificant, in the ophthalmic artery beside die central retinal and short posterior ciliary arteries.

Because the anterior ciliary arteries are a major source of blood supply to die anterior segment of the eye and are transected during strabismus surgery, anterior segment ischemia may occur as a result of inadequate blood supply postoperatively on three or four rectus muscles. Surgery on one or two rectus muscles is common in ophthalmic practice and poses virtually no risk for anterior segment ischemia in an otherwise healthy patient. Transient abnormalities in iris circulation occur after tenotomy of a previously unoperated vertical, but not horizontal, rectus muscle.5'7 A previously tenotomized rectus muscle does not reestablish communication with the anterior ciliary circulation.8 Therefore, one may think that this will result in hemodynamic changes in the ophdialmic artery.

This study evaluated hemodynamic changes in the ophdialmic artery with color Doppler ultrasonography in patients who underwent strabismus surgery (recession or resection) on two horizontal rectus muscles in one eye.

MATERIALS AND METHODS

Nineteen patients who underwent strabismus surgery comprised the study group. Measurements from both eyes of 16 normal age- and sex-matched subjects served as normal data. Inclusion criteria required that patients had no previous surgery in either eye. Patients with a systemic disease such as diabetes mellitus, hypertension, and blood dyscrasia, which can affect the results of velocity and resistance measurements, were excluded from the study.

Eighteen eyes of 18 patients who underwent recession or resection surgery on two horizontal rectus muscles in one eye and both eyes of a patient who underwent recession surgery on two horizontal rectus muscles in each eye were evaluated with color Doppler ultrasonography preoperatively and 1 week and 1 mondi postoperatively. Postoperative medications included fluorometholone 1% and antibiotic drops without other medications.

An Acuson 128 XF CDI unit (Mountain-view, Calif) with a 7-mHz linear-phased transducer was used to examine all eyes in die mediod oudined previously.9 Informed consent was obtained from all study and control subjects. Doppler frequency shifts within the ophthalmic artery were measured to determine systolic maximum, end-diastolic, and mean velocities (in centimeters per second). The resistance index was calculated using die following equation: systolic maximum velocity-end-diastolic velocity/systolic maximum velocity.10 Velocity measurements are dependent on the beam-vessel angle, whereas the resistance index is angle-independent because it is a ratio.

All measurements were performed by die same specialist (K.M. Y.) experienced with CDI for orbital blood flow. The systolic maximum velocity, mean velocity, end-diastolic velocity, pulsatility index, and resistance index of die ophdialmic artery were determined. The Mann- Whitney U test was used to compare preoperative measurements in the study and control eyes. Statistical comparison between preoperative and postoperative measurements in the study group was performed using Friedman's two-way analysis of variance.

RESULTS

Mean age was 26.8 ±6.4 years (range: 18-42 years) in the study group and 25.7±5.3 years (range: 16-41 years) in the control group. There were 11 men and 8 women in the study group, and 12 men and 9 women in the control group.

No significant difference was noted in preoperative blood flow velocities or vascular resistance between study and control eyes (Table 1). Color Doppler waveforms generally showed slight changes in amplitude and shape after strabismus surgery on two horizontal rectus muscles in one eye, whereas a few cases demonstrated a notable increase, particularly in systemic maximum velocity, 1 mondi postoperatively compared to the preoperative value (Figure).

Table

TABLE 1COMPARISON OF MEAN (±SD) PREOPERATIVE HEMODYNAMIC PARAMETERS IN THE OPHTHALMIC ARTERY IN THE CONTROL AND STUDY GROUPS

TABLE 1

COMPARISON OF MEAN (±SD) PREOPERATIVE HEMODYNAMIC PARAMETERS IN THE OPHTHALMIC ARTERY IN THE CONTROL AND STUDY GROUPS

Figure: Color Doppler waveforms showing a marked increase in systolic maximum velocity (big arrow) and end-diastolic velocity (small arrow) preoperatively (A) and 1 month postoperatively (B) on two horizontal rectus muscles in one eye.

Figure: Color Doppler waveforms showing a marked increase in systolic maximum velocity (big arrow) and end-diastolic velocity (small arrow) preoperatively (A) and 1 month postoperatively (B) on two horizontal rectus muscles in one eye.

The clinical characteristics and color Doppler ultrasonography results for each patient in the study group are shown in Table 2. In the study group, die ophdialmic artery showed a slight but not significant increase in systemic maximum velocity 1 month postoperatively compared to preoperative measurements. Differences between preoperative and postoperative mean velocity, end-diastolic velocity, pulsatility index, and resistance index in the ophdialmic artery also were not statistically significant (Table 3).

DISCUSSION

The major blood supply to the eye originates from the ophthalmic artery. Circulation to the anterior segment, including the iris and ciliary body, is maintained through the long posterior and anterior ciliary arteries. The two long posterior ciliary arteries having an intrascleral course beneath the horizontal rectus muscles are estimated to provide <30% of die blood supply to the anterior segment of the eye."11,12 Despite common anatomical variations,13 the medial rectus and both vertical rectus muscles typically carry two anterior ciliary arteries travelling extraocularly, but the lateral rectus muscle carries only one.14 Animal studies indicate that 70%-80% of the blood supply to the anterior segment is contributed by the anterior ciliary system.12 Thus, occlusion of the long posterior ciliary arteries alone produces no ischemic changes, indicating diese vessels are not needed to maintain adequate blood supply to the anterior segment.1115

Obviously, surgical manipulation of the rectus muscles poses the greater risk for ischemic injury. However, the extensive collateral vascular supply to the anterior segment probably accounts for the relative rarity of anterior segment ischemia after surgery on extraocular muscles.16 It has gradually become apparent that both patient susceptibility and the extent of strabismus surgery are major variables in the production of anterior segment ischemia. While the most important risk factor is age, particularly in patients undergoing surgery on one or both vertical rectus muscles,16"18 circulatory disorders such as adierosclerosis, blood dyscrasia, and carotid artery disease also appear to add substantially increased risk.16'19'21

Table

TABLE 2CLINICAL CHARACTERISTICS AND COLOR DOPPLER ULTRASONOGRAPHY RESULTS OF THE STUDY GROUP PATIENTS

TABLE 2

CLINICAL CHARACTERISTICS AND COLOR DOPPLER ULTRASONOGRAPHY RESULTS OF THE STUDY GROUP PATIENTS

Table

TABLE 3MEAN (±SD) BLOOD FLOW MEASURES FOR THE OPHTHALMIC ARTERY IN THE STUDY GROUP

TABLE 3

MEAN (±SD) BLOOD FLOW MEASURES FOR THE OPHTHALMIC ARTERY IN THE STUDY GROUP

Fluorescein angiography of the anterior segment has been a useful research tool for studying the normal anterior segment circulation and specific disease processes.515,22,23 Iris fluorescein angiography, although not necessary for clinical diagnosis, is useful for evaluating anterior segment circulation, particularly in anterior segment ischemia. Filling delays can be demonstrated not only in eyes of patients with clinical signs of anterior segment ischemia, but also in clinically normal eyes after tenotomy of a single vertical rectus muscle, eidier in isolation or in combination with horizontal rectus muscle surgery.6,7,24

Perfusion defects identified with iris fluorescein angiography tend to be a greater area of involvement, and longer filling delays are produced by surgery on multiple rectus muscles. Iris filling defects improve rapidly following surgery and are rarely permanent.6'7,11,24 Previously tenotomized rectus muscles probably do not reestablish communication with the anterior ciliary circulation,8 and repeat operations do not produce angiographically detectable changes in iris circulation,6,7 thus posing no additional risk to the patient for producing anterior segment ischemia.20 This may result from the fact that indocyanine green angiography was not performed in any of those studies. Because indocyanine green angiography was reported to provide angiographic visualization of deeper stromal iris vessels and also minor arterial circle particularly in darkly pigmented irides that were not detected by fluorescein angiography, it has become a useful means to study the structure and the hemodynamics of the iris and anterior ciliary vessels.25,26

Anorher explanation may be other potential routes of blood supply, especially via die posterior ciliary arteries and conjunctival perilimbal Tenons plexus. On the other hand, both the number and combination of rectus muscles that can be operated on safely at one time remains controversial.11,19"21 However, detachment of the medial and lateral rectus muscle in a previously unoperated eye poses no risk for anterior segment ischemia in a healthy patient.24

All of these changes studied by fluorescein angiography of the anterior segment necessarily will produce an idea that hemodynamic changes in anterior segment circulation, particularly in anterior ciliary arteries, may occur after surgery on rectus muscles. Color Doppler ultrasonography is a relatively new method that has been used in ocular blood flow studies.27 Reasonable changes in ocular and orbital blood flow have been detected with color Doppler ultrasonography after retinal detachment surgery, trabeculectomy, and a variety of ocular diseases such as glaucoma, retinitis pigmentosa, degenerative myopia, age-related macular degeneration, and diabetic retinopathy.1,3,28"31 However, the use of color Doppler ultrasonography for retrobulbar hemodynamic changes after strabismus surgery has not been reported before. Thus, our study may represent a new point of view for die hemodynamic changes occurring after strabismus surgery.

Iris angiography is a useful but invasive method for studying the anterior segment circulation after strabismus surgery. On the other hand, color Doppler ultrasonography, which is noninvasive and carries no potential risk for the patient, may be a new approach in this field. The major limitation here is that anterior ciliary arteries are not large enough to be visualized accurately. However, as the origin of anterior ciliary arteries is the ophthalmic artery, it would be appropriate to evaluate the possible reflections in hemodynamic alterations in the ophdialmic artery after surgery on rectus muscles.

Our study showed slight changes in amplitude and shape of Doppler waveforms after two horizontal rectus surgeries in one eye. The Ophthalmie artery, while showing a slight increase in systolic maximum velocity 1 month postoperatively compared to the preoperative measures, achieved no statistical significance in any postoperative interval for all flow parameters. The results suggest diat two horizontal rectus surgeries in a previously unoperated eye do not cause significant changes in the ophdialmic artery. This appears to agree with the results of previous stuthes.6,711'24 As explained previously, surgery on vertical rectus muscles in one eye may possibly have an effect on orbital circulation, and color Doppler ultrasonography will be helpful in evaluating these flow changes.

In this study, preoperative hemodynamic parameters in the ophthalmic artery between the study and control eyes demonstrated no significant differences. Therefore, we considered diat our study group was not different from the age- and sexmatched control subjects, and dius the comparisons between preoperative and postoperative results in the study eyes were adequately accurate and reliable. The relative lack of significant changes in flow parameters of the ophthalmic artery might be explained by the fact that the anterior ciliary arteries make up only a portion of its total distribution. On the other hand, there may be different contributory factors on the results of flow measurements in the ophthalmic artery. In addition, the physiologic variation of the parameters measured over time is not known,3 whereas the results of this technique in the assessment of orbital blood flow have been reported to be reproducible.32,33

Formal stuthes are critical to better understand the physiologic variation of the parameters in orbital circulation in health and disease. Some characteristics, especially the resistance of the circulatory system, may vary depending on the location. For example, the ocular circulation, as well as the carotid and placental circulation, generally are considered low-resistance systems, whereas circulation of the leg and mesenteric circulation are defined as high-resistance systems that have varying resistance depending on the activity level such as exercise and activity of the digestive system.3

CONCLUSION

Our findings showed slight but not significant hemodynamic changes in ophdialmic artery circulation after two horizontal rectus muscle surgeries. Further studies are needed to better understand rhe effect of rectus muscles surgery with various combinations on retrobulbar blood flow.

REFERENCES

1. Regillo CD, Sergoc RC, Brown GC. Successiti) scierai budding procedures decrease central retinal artery blood flow velocity. Ophthalmology 1993;100:1044-1049.

2. Santos L, Capeans C, Gonzalez F, et al. Ocular blood flow velocity reduction after buckling surgery. Graefes Arch Clin Exp Ophthalmol 1994;232:666-669.

3. Trible JR, Sergott RC, Spaeth GL, et al. Trabeculectomy is associated wich retrobulbar hemodynamic changes: a color Doppler analysis. Ophthalmology 1994;101:340-351.

4. Mirtra RA, Sergott RC, Flaharty PM, et al. Optic nerve decompression improves hemodynamic parameters in papilledema. Ophthalmology 1993;10O: 987-997.

5. Hayreh SS, Scott WE. Fluorescein iris angiography, I: normal pattern. Arch Ophthalmol 1978;96:1383-1389.

6. Oivcr JM, Lcc JP. Recovery of anterior segment circulation after strabismus surgery in adult patients. Ophthalmology 1992;99:305-315.

7. Olver JM, Lee JP. The effects of strabismus surgery on anterior segment circulation. Eye. 1989;3:318-326.

8. Olver JM, McCartney AC, Lee JP. The strabismic scar: a microvascular corrosion cast study. Journal of Optometry and Physiological Optics. 1989;30(suppl):377. Abstract.

9. Lieb WE, Cohen SM, Merton DA, et al. Color Doppler imaging of the eye and orbit: technique and normal vascular anatomy. Arch Ophthalmol 1991;109:527-531.

10. Planiol Th, Pourcelot L, Pettier J-M, Degiovanni E. Étude de la circulation carotithenne par les méthodes ultrasoniques et la thermographie. Reo Neurol 1972;126:127-141.

11. Vîrdi PS, Hayreh SS. Anterior segment ischemia after recession of various recti: an experimental study. Ophthalmology 1 987:94: 12581271.

12. Wilcox LM, Keough EM, Connally RJ, Hone CE. The contribution of blood flow by anterior ciliary arteries to the anterior segment in the primate eye. Exp Eye Res. 1980;30:167-174.

13. McKeown CA, Lambert HM, Shore JW. Preservation of anterior ciliary vessels during extraocular muscle surgery. Ophthalmology 1989;96:498-506.

14. Duke-Elder S. System of Ophthalmology. Vol 2. London. England: Henry Kimpton; 1961.

15. Hayreh SS. Anatomy and pathophysiology of ocular circulation. Exp Eye Res. 1973;17:387-404.

1 6. France TD, Simon JW. Anterior segment ischemia syndrome following muscle surgery. The AAPOS experience. J Pediatr Ophthalmol Strabismus. 1986;23:87-91.

17. Elsas FJ, Withcrspoon CD. Anterior segment ischemia after strabismus surgery in a child. AmJ Ophthalmol 1987;6:833-834.

1 8. Hiatt RL Production of anterior segment ischemia. Trans Am Ophthalmol Soc. 1977;75:87-102.

19. Saunders RA, Sandall GS. Anterior segment ischemia syndrome following rectus muscle transposition. Am J Ophthalmol 1982;93:34-38.

20. Simon JW, Price EC, Krohel GB, et al. Anterior segment ischemia following strabismus surgery. J Pediatr Ophthalmol Strabismus. 1984;21:179-184.

21. Wagner RS, Nelson LR. Complications following strabismus surgery. Int Ophthalmol Clin. 1985;25:171-178.

22. Meyer PA, Watson PG. Low dose fluorescein angiography of the conjunctiva and episcleral. Br J Ophthalmol 1987;71:2-10.

23. Ormerod LD, Fariza E, Hughes GW, et al. Anterior segment fluorescein videoangiography with a scanning angiographic microscope. Ophthalmology 1990;97:745-751.

24. Hayreh SS, Scott .WE. Fluorescein iris angiography, II: disturbances in iris circulation following strabismus operation on the various recti. Arch Ophthalmol 1978;96:1390-1400.

25. Podgornaia NN, Akhmedov AA. Indocyanine green fluorescence iridoangiography in pigmented iris. Vestn OfiabnoL 1991;107:40-43.

26. Maruyama Y, Kishi S, Kamei Y, Shimizu R, Kimura Y. Infrared angiography of the anterior ocular segment. Surv Ophthalmol 1995;39:40-48.

27. Aburn NS, Sergott RC. Orbital color Doppler imaging. Eye. 1993;7:639-647.

28. Akyol N, Kiikner S, Celiker Ü, Kbyu H, Lüleci C. Decreased retinal blood flow in retinitis pigmentosa. Can J Ophthalmol 1995;30:28-32.

29. Friedman E, Krupsky S, Lane AM. Ocular blood flow velocity in age related macular degeneration. Ophthalmology. 1995:102:640646.

30. Goebel W, Lieb WE, Ho A, Sergott RC, Farhoumand R, Grehn F. Color Doppler imaging: a new technique to assess orbital flow in patients with diabetic retinopathy. Invest Ophthalmol Vis Sci. 1995;36:864-870.

31. Akyol N. Kükner S, Özdemir T, Esmerligil S. Choroidal and retinal blood flow changes in degenerative myopia. Can J Ophthalmol 1996;31:113-119.

32. Williamson TH, Harris A, Shoemaker JA, et al. Reproducibility of color Doppler imaging assessment of blood flow velocity in orbital vessels. Invest Ophthalmol Vis Sci. 1994;35(suppl):l658. Abstract.

33. Rojanapongpun P, Morino B, Drance SM. Reproducibility of transcranial Doppler ultrasound examinations of the ophthalmic artery flow velocity. BrJ Ophthalmol 1993;77:22-24.

TABLE 1

COMPARISON OF MEAN (±SD) PREOPERATIVE HEMODYNAMIC PARAMETERS IN THE OPHTHALMIC ARTERY IN THE CONTROL AND STUDY GROUPS

TABLE 2

CLINICAL CHARACTERISTICS AND COLOR DOPPLER ULTRASONOGRAPHY RESULTS OF THE STUDY GROUP PATIENTS

TABLE 3

MEAN (±SD) BLOOD FLOW MEASURES FOR THE OPHTHALMIC ARTERY IN THE STUDY GROUP

10.3928/0191-3913-20000301-08

Sign up to receive

Journal E-contents