- Email: [email protected]
Quantitative measurement of retinal vascular diameter changes in the early postoperative period after strabismus surgery
Accepted Manuscript Quantitative measurement for the retinal vascular diameter changes in the early postoperative period after strabismus surgery Jinqiong Zhou, MD, PhD, Jing Fu, MD, PhD, Jipeng Li, MD, PhD, Xiaozhen Wang, MD, PhD, Wenying Wang, MD, PhD, Bowen Zhao, MD, PhD, Meng Qi, MD, PhD PII:
S1091-8531(16)30774-1
DOI:
10.1016/j.jaapos.2017.04.004
Reference:
YMPA 2636
To appear in:
Journal of AAPOS
Received Date: 20 December 2016 Revised Date:
3 April 2017
Accepted Date: 6 April 2017
Please cite this article as: Zhou J, Fu J, Li J, Wang X, Wang W, Zhao B, Qi M, Quantitative measurement for the retinal vascular diameter changes in the early postoperative period after strabismus surgery, Journal of AAPOS (2017), doi: 10.1016/j.jaapos.2017.04.004. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Quantitative measurement for the retinal vascular diameter changes in the early postoperative period after strabismus surgery Jinqiong Zhou, MD, PhD, Jing Fu, MD, PhD, Jipeng Li, MD, PhD, Xiaozhen Wang, MD, PhD, Wenying Wang, MD, PhD, Bowen Zhao, MD, PhD, and Meng Qi, MD, PhD Author affiliations: Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University; Beijing Ophthalmology & Visual Sciences Key Laboratory, Beijing, China
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Supported by the Project for Collaboration between Basic Science and Clinical Practice of Capital Medical University. Submitted December 20, 2016. Revision accepted April 5, 2017.
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Correspondence: Prof. Jing Fu, MD, Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University; Beijing Ophthalmology & Visual Sciences Key Laboratory, Beijing 100730, China (email: [email protected]).
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Word count: 1,900 Abstract only: 189
ACCEPTED MANUSCRIPT Abstract Purpose To investigate quantitatively the retinal vascular diameter changes before and after strabismus surgery, analyzing the potential hemodynamic changes that may occur in the retinal
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circulation. Methods
Consecutive patients with horizontal strabismus who underwent strabismus surgery were
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prospectively enrolled. Color fundus photographs were taken of each eye before and 1 day after surgery. The retinal vessel diameters were measured using computer-assisted
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quantitative assessment software. Paired-sample t test was used to evaluate the central retinal arteriolar equivalent (CRAE), central retinal venular equivalent (CRVE), and arteriovenous ratio (AVR) before and 1 day after surgery. We also analyzed those changes in different subgroups according to surgical protocols.
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Results
A total of 217 eyes of 148 patients were included. Compared with the data before surgery, the mean CRAE significantly increased 1 day after surgery (P = 0.01), so did the AVR (P =
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0.003). There was no significant difference with respect to CRVE (P = 0.43). The CRAE and AVR were not significantly different in the lateral rectus recession group.
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Conclusions
Strabismus surgery on horizontal rectus muscles may change retinal hemodynamics by increasing the central retinal arteriolar diameter during the early postoperative period.
ACCEPTED MANUSCRIPT The blood supply for 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, which have an intrascleral course beneath the horizontal rectus muscles, are estimated to provide less than 30% of the blood supply to the anterior segment of the eye.1,2 The other
which come from the arteries of the rectus muscles.1,3
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70%-80% of the anterior segment blood supply is provided by the anterior ciliary arteries,
Because the anterior ciliary arteries are the major source of blood supply to the
SC
anterior segment of the eye and are transected during strabismus surgery, anterior segment ischemia may occur as a result of inadequate blood supply postoperatively. Surgery on one or
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two rectus muscles is common in ophthalmic practice and poses virtually no risk for anterior segment ischemia in healthy patients, but the hemodynamic effect on the anterior segment is still unclear. In addition, because the long posterior ciliary arteries, anterior ciliary arteries, and retinal artery originate from the ophthalmic artery, some hemodynamic changes may occur in the retinal circulation due to the increased blood flow of the anterior segment after
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strabismus surgery.4-6 The consequence of reduced anterior segment perfusion on blood flow in the posterior ciliary arteries, retinal arteries, and the ophthalmic artery is unknown.
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Several studies using color Doppler ultrasonography to assess the orbital blood flow changes after strabismus surgery have shown conflicting results in terms of whether or not
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the blood flow of ophthalmic artery might increase.4,6-8 However, orbital Doppler ultrasonography is a user-dependent and time-consuming imaging method, in which complete patient cooperation is essential. In addition, these studies reported quite small number of patients with short-term observation after surgery. Recently, a semiautomated system was developed to measure retinal vessel diameters in vivo noninvasively, with good reliability and repeatability.9 Population-based studies using the semiautomated system have shown that retinal vascular diameter changes may be associated with clinical hypertension,10 coronary artery disease,11 and stroke.12 The current
ACCEPTED MANUSCRIPT study used this computer-assisted quantitative assessment software to evaluate the retinal vascular diameter changes before and 1 day after strabismus surgery with the aim of analyzing potential hemodynamic changes that may occur in retinal circulation after strabismus surgery.
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Subjects and Methods
The Medical Ethics Committee of Beijing Tongren Hospital approved the study protocol, and written informed consent was obtained from all the patients. A total of 156 consecutive
SC
patients with horizontal strabismus who underwent rectus muscle surgery between January 2014 and August 2015 at Beijing Tongren Eye Center were enrolled prospectively. The
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diagnosis of strabismus was made by an experienced surgeon (JF) after detailed examination. Color fundus photographs were taken preoperatively and 1 day after surgery. Slit-lamp examination focused on signs of anterior segment ischemia, characterized by pupillary dilation and distortion, iris atrophy, lens opacities, and hypotonia.7 Patients were divided into
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different groups based on which rectus muscle was transected. Patients were excluded if they had undergone previous anterior or posterior ocular surgery, had systematic diseases (such as diabetes mellitus, systemic hypertension, or any other known vascular diseases), or had
EP
vertical strabismus that required surgery on oblique muscles. Recession and resection were performed using the standard method and involved
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transecting the anterior ciliary arteries. All surgical interventions were performed under general anesthesia by the same experienced surgeon (JF). A limbal conjunctival incision was used in all patients. Following reattachment of the rectus muscle, the conjunctiva was sutured with 6-0 absorbable sutures. Color fundus photographs (45°) of each eye were taken using the CR6-45NM fundus camera (Canon Inc, Japan, Tokyo) centered on the optic disk (Diabetic Retinopathy Study standard field 1) and macula (Diabetic Retinopathy Study standard field 2) before and 1 day after strabismus surgery.13
ACCEPTED MANUSCRIPT To assess retinal vascular caliber changes, the retinal vessel diameters were measured using computer-assisted quantitative assessment software (IVAN; University of Wisconsin, Madison, WI), as described and applied in previous population-based studies.9,10 Average retinal arteriolar or venular width was calculated by means of the Parr-Hubbard formula as
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the central retinal arteriolar equivalent (CRAE) or central retinal venular equivalent (CRVE). The arteriovenous ratio (AVR) was calculated as CRAE divided by CRVE.14,15 Statistical Analysis
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Statistical analysis was performed using SPSS for Windows, version 22.0 (IBM-SPSS,
Chicago, IL). In a first step, we determined the mean values (with standard deviation) and
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median values of the main outcome parameters. In a second step, we performed paired-samples t test analyses to evaluate the changes of the CRAE, CRVE, and the AVR before and 1 day after the strabismus surgery. A P value of <0.05 was considered significant. Results
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Of the 156 consecutive patients, 8 patients were excluded because of poor-quality pre- or postoperative fundus photographs. The poor quality was due to lack of cooperation in 6 patients and persistent ointment after surgery in 2 patients. A total of 217 eyes of 148 patients
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(74 males [50%]) were included in the analysis. Mean subject age was 13.33 ± 9.52 years (range, 3-51years). Strabismus surgery was performed for exotropia in = 112 cases and
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esotropia in36 cases.
In all 217 no sign of anterior segment ischemia (such as iritis, pupil distortion,
keratitis, irregularity of descemet’s memebrane, posterior synechiae, corneal or iridial neovascularization, rubeosis, cataract, or hypotonia) was found pre- or postoperatively. The mean CRAE at postoperative day 1 was significantly larger than preoperative value (130.64 ± 28.57 vs 124.77 ± 27.21 [P = 0.01]). The mean CRVE at postoperative day 1 did not differ significantly from the preoperative value (174.50 ± 35.35 vs 172.29 ± 31.73 [P = 0.427]). The AVR at postoperative day 1 was significantly larger than preoperative value (0.75 ± 0.09 vs
ACCEPTED MANUSCRIPT 0.73 ± 0.11 [P = 0.003]). See Table 1. We also analyzed the 79 unoperated fellow eyes for comparison and found no clinically significant changes postoperatively no significant difference before surgery and at day 1 after surgery in terms of CRAE (128.97 ± 28.06 vs 132.63 ± 25.86 [P = 0.31]), CRVE
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(173.75 ± 32.80 vs 175.23 ± 32.23 [P = 0.75]), or AVR (0.75 ± 0.10 vs 0.76 ± 0.01 [P = 0.16]).
Of the 217 eyes, 117 eyes (53.9%) underwent surgery with only one rectus muscle
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recession. The other 100 eyes underwent both medial and lateral rectus surgery. For both these groups, significant increase of CRAE and AVR was found. However, further subgroup
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analysis for one rectus surgery group showed significant increase of CRAE and AVR only in the medial rectus recession but not in the lateral rectus recession group. Detailed results of the changes of the retinal vascular caliber before and after surgery are provided in Table 2. Discussion
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Computer-assisted quantitative assessment software (IVAN; University of Wisconsin, Madison, WI) has been used to measure the retinal vascular caliber to evaluate the blood flow and the hemodynamic alterations related to certain ophthalmologic and orbital diseases for
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more than 10 years with great reliability and repeatability.9 This noninvasive imaging method has also been used to demonstrate the potential hemodynamic changes of systemic diseases
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such as hypertension, stroke, and diabetes, with conflicting results. In the current study, we used this noninvasive imaging method to analyze the potential effects of strabismus surgery on retinal circulation. Our study analyzed the retinal vascular diameter changes before and 1 day after strabismus surgery in a large series of strabismus patients, with a mean age of 13.07 years. Anterior segment ischemia is a rare but serious complication of strabismus surgery, with a reported incidence of 1/13,000.16-18 In our study there were no signs of anterior segment ischemia pre- or postoperatively.
ACCEPTED MANUSCRIPT As we hypothesized, after the recession or resection of rectus muscles, some hemodynamic changes in retinal circulation may occur because of increased blood flow demands of the anterior segment.4-6 Our study showed that 1 day after surgery CRAE significantly increased compared to the preoperative value (P = 0.01), as did the
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arteriovenous ratio (P = 0.003). These results suggest that strabismus surgeons should consider retinal circulation status when planning strabismus surgeries, particularly for
patients at risk of retinal vascular diseases, such as diabetic patients. There was no significant
SC
change of the retinal venular diameter (CRVE, P = 0. 43). This result is consistent with a study by Lee and colleagues19 that showed that surgery on two horizontal rectus muscles
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increased ophthalmic artery blood flow during the early postoperative period (1 day) but returned to normal at day 7 or later, as measured by color Doppler imaging. Bayramlar and colleagues4 revealed that color Doppler ultrasound measurements did not show significant change in ophthalmic artery at 1 week and 1 month after surgery on two horizontal rectus
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muscles. But they did not measure the blood flow 1 day after surgery. Retinal venular diameters have been reported to be less sensitive for the retinal blood flow changes,3,6 which may be related to the role of autoregulation played by the retinal
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capillary and explain the unchanged CRVE in the present study. Further studies dealing with the late stage of retinal vascular changes are indicated.
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Our study also found that when classified into two groups according to rectus muscles, significant increase of CRAE and AVR was only found in medial rectus recession but not in lateral rectus recession. This is likely due to the fact that the medial rectus and both vertical rectus muscles typically carry two anterior ciliary arteries, whereas the lateral rectus muscle carries only one. This result suggests that at least two anterior ciliary arteries injuries are needed to cause changes in retinal blood flow, and the lateral rectus muscle cut off played a minor role in postoperative change in retina blood flow. There are potential limitations to the generalizability of our results. First, referral bias
ACCEPTED MANUSCRIPT cannot be ruled out. Second, the retinal vascular diameters were assessed on routinely taken fundus photographs, which may lead overlooking of the systolic or diastolic effect on retinal vascular diameter. In conclusion, our results showed that strabismus surgery on horizontal rectus muscles
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may increase retinal blood flow during the early postoperative period. We also found that, surgery on the lateral rectus muscle played a minor role on postoperative retinal blood flow, because it carries only one anterior ciliary artery. Further studies would be needed to analyze
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hemodynamics of vertical rectus muscle transection.
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the retinal vascular changes at a later stage after strabismus surgery and the effect on retinal
ACCEPTED MANUSCRIPT References 1.
Virdi PS, Heyreh SS. Anterior segment ischemia after recession of various recti. An experimental study. Ophthalmology 1987;94:1258-71.
2.
Wilcox LM, Keough EM, Connolly RJ, Hotte CE. The contribution of blood flow by
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anterior ciliary arteries to the anterior segment in the primate eye. ExP Eye Res 1980;30:167-74. 3.
Hayreh SS. Proceedings: anatomy and pathophysiology of ocular circulation. ExP
4.
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Eye Res 1973;17:387-8.
Bayramlar H, Totan Y, Çekiç O, Yazıcıoğlu KM, Aydın E. Evaluation of
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hemodynamic changes in the ophthalmic artery with color Doppler ultrasonography after strabismus surgery. J Pediatr Ophthalmol Strabismus 2000;37:94-100. 5.
Güven DM, Zıraman IM˙, Tomaç SM, Sancak DM, Karaemir MA, Hasıripi H. Hemodynamic changes after strabismus surgery. Strabismus 2000;8:21-7. Pelit A, Barutçu Ö, Oto S, Aydın P. Investigation of hemodynamic changes after
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6.
strabismus surgery using color Doppler imaging. J AAPOS 2002;6:224-7. 7.
Akyüz Unsal AI, Unsal A, Ozkan SB, Karaman CZ. The effect of strabismus surgery
8.
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on retrobulbar hemodynamics. J AAPOS 2007;11:277-81. Lee NH, Lee SN. Investigation of hemodynamic changes in the ophthalmic artery
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using color doppler imaging after strabismus surgery. Kor J Ophthalmol 2005;19:208-12.
9.
Wong TY, Knudtson MD, Klein R, Klein BE, Meuer SM, Hubbard LD.
Computer-assisted measurement of retinal vessel diameters in the Beaver Dam Eye Study: methodology, correlation between eyes, and effect of refractive errors. Ophthalmology 2004;111:1183-90.
10.
Kawasaki R1, Cheung N, Wang JJ, et al. Retinal vessel diameters and risk of hypertension: the Multiethnic Study of Atherosclerosis. J Hypertens 2009;27:2386-93.
ACCEPTED MANUSCRIPT 11.
Wang S, Xu L, Jonas JB, et al. Major eye diseases and risk factors associated with systemic hypertension in an adult Chinese population: the Beijing Eye Study. Ophthalmology 2009;116:2373-80.
12.
Wong TY, Klein R, Couper DJ, et al. Retinal microvascular abnormalities and incident
13.
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stroke: the Atherosclerosis Risk in Communities Study. Lancet 2001;358:1134-40. Zhou J, Xu L, Wang S, et al. The 10-year incidence and risk factors of retinal vein occlusion: the Beijing Eye Study. Ophthalmology 2013;120:803-8.
Knudtson M, Lee K, Hubbard L, et al. Revised formulas for summarizing retinal vessel diameters. Curr Eye Res, 2003;27:143-9.
Xu L, Zhou J, Wang S, et al. Localized retinal nerve fiber layer defects and arterial
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15.
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14.
hypertension. Am J Hypertens 2013;26:511-17. 16.
Lee JP, Olver JM. Anterior segment ischemia following vertical muscle transposition and botulinum toxin injection. Arch Ophthalmol 1991;109:174. Stucchi C, Bianchi G. Depigmentation in the iris sector following muscle
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17.
transplantations. Ophthalmologica 1957;133:231-6. 18.
France TD, Simon JW. Anterior segment ischemia syndrome following muscle
Lee NH, Lee SN. Investigation of hemodynamic changes in the ophthalmic artery using color Doppler imaging after strabismus surgery. Korean J Ophthalmol
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19.
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surgery: the AAPOS experience. J Pediatr Ophthalmol Strabismus 1986;23:87-91.
2005;19:208-12.
ACCEPTED MANUSCRIPT
Preoperative Postoperative t P value
CRAE 124.77 ± 27.28 130.64 ± 28.57 −2.517 0.013
CRVE AVR 172.29 ± 31.73 0.73 ± 0.11 174.50 ± 35.35 0.75 ± 0.09 −0.796 −3.016 0.427 0.003
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AVR, arteriovenous ratio; CRAE, central retinal arteriolar equivalent; CRVE, central retinal venular equivalent.
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Table 1. Characteristics and comparison of retinal vessels caliber before and after surgery of all 217 eyes
ACCEPTED MANUSCRIPT
Table 2. Comparison of retinal vessels caliber preoperative and postoperative for eyes with one rectus muscle recession
LR recess (n = 87)
CRAE 123.88 ± 24.58 130.05 ± 27.49 −2.089 0.039 124.73 ± 22.99 136.32 ± 31.77 −1.842 0.036 123.59 ± 25.23 127.89 ± 25.70 −1.293 0.199
CRVE 170.90 ± 29.95 172.15 ± 33.84 −0.363 0.718 173.25 ± 30.10 180.29 ± 39.04 −0.854 0.400 170.10 ± 30.03 169.34 ± 31.62 0.208 0.836
AVR 0.73 ± 0.10 0.76 ± 0.09 −2.915 0.004 0.72 ± 0.08 0.76 ± 0.09 −2.661 0.013 0.73 ± 0.11 0.76 ± 0.09 −2.146 0.035
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MR recess (n = 30)
Time Preoperative Postoperative t P value Preoperative Postoperative t P value Preoperative Postoperative t P value
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Surgical method One rectus muscle recess (n = 117)
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AVR, arteriovenous ratio; CRAE, central retinal arteriolar equivalent; CRVE, central retinal venular equivalent; LR, lateral rectus muscle; MR, medial rectus muscle; Recess, recession.
S1091-8531(16)30774-1
DOI:
10.1016/j.jaapos.2017.04.004
Reference:
YMPA 2636
To appear in:
Journal of AAPOS
Received Date: 20 December 2016 Revised Date:
3 April 2017
Accepted Date: 6 April 2017
Please cite this article as: Zhou J, Fu J, Li J, Wang X, Wang W, Zhao B, Qi M, Quantitative measurement for the retinal vascular diameter changes in the early postoperative period after strabismus surgery, Journal of AAPOS (2017), doi: 10.1016/j.jaapos.2017.04.004. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Quantitative measurement for the retinal vascular diameter changes in the early postoperative period after strabismus surgery Jinqiong Zhou, MD, PhD, Jing Fu, MD, PhD, Jipeng Li, MD, PhD, Xiaozhen Wang, MD, PhD, Wenying Wang, MD, PhD, Bowen Zhao, MD, PhD, and Meng Qi, MD, PhD Author affiliations: Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University; Beijing Ophthalmology & Visual Sciences Key Laboratory, Beijing, China
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Supported by the Project for Collaboration between Basic Science and Clinical Practice of Capital Medical University. Submitted December 20, 2016. Revision accepted April 5, 2017.
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Correspondence: Prof. Jing Fu, MD, Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University; Beijing Ophthalmology & Visual Sciences Key Laboratory, Beijing 100730, China (email: [email protected]).
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Word count: 1,900 Abstract only: 189
ACCEPTED MANUSCRIPT Abstract Purpose To investigate quantitatively the retinal vascular diameter changes before and after strabismus surgery, analyzing the potential hemodynamic changes that may occur in the retinal
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circulation. Methods
Consecutive patients with horizontal strabismus who underwent strabismus surgery were
SC
prospectively enrolled. Color fundus photographs were taken of each eye before and 1 day after surgery. The retinal vessel diameters were measured using computer-assisted
M AN U
quantitative assessment software. Paired-sample t test was used to evaluate the central retinal arteriolar equivalent (CRAE), central retinal venular equivalent (CRVE), and arteriovenous ratio (AVR) before and 1 day after surgery. We also analyzed those changes in different subgroups according to surgical protocols.
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Results
A total of 217 eyes of 148 patients were included. Compared with the data before surgery, the mean CRAE significantly increased 1 day after surgery (P = 0.01), so did the AVR (P =
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0.003). There was no significant difference with respect to CRVE (P = 0.43). The CRAE and AVR were not significantly different in the lateral rectus recession group.
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Conclusions
Strabismus surgery on horizontal rectus muscles may change retinal hemodynamics by increasing the central retinal arteriolar diameter during the early postoperative period.
ACCEPTED MANUSCRIPT The blood supply for 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, which have an intrascleral course beneath the horizontal rectus muscles, are estimated to provide less than 30% of the blood supply to the anterior segment of the eye.1,2 The other
which come from the arteries of the rectus muscles.1,3
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70%-80% of the anterior segment blood supply is provided by the anterior ciliary arteries,
Because the anterior ciliary arteries are the major source of blood supply to the
SC
anterior segment of the eye and are transected during strabismus surgery, anterior segment ischemia may occur as a result of inadequate blood supply postoperatively. Surgery on one or
M AN U
two rectus muscles is common in ophthalmic practice and poses virtually no risk for anterior segment ischemia in healthy patients, but the hemodynamic effect on the anterior segment is still unclear. In addition, because the long posterior ciliary arteries, anterior ciliary arteries, and retinal artery originate from the ophthalmic artery, some hemodynamic changes may occur in the retinal circulation due to the increased blood flow of the anterior segment after
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strabismus surgery.4-6 The consequence of reduced anterior segment perfusion on blood flow in the posterior ciliary arteries, retinal arteries, and the ophthalmic artery is unknown.
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Several studies using color Doppler ultrasonography to assess the orbital blood flow changes after strabismus surgery have shown conflicting results in terms of whether or not
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the blood flow of ophthalmic artery might increase.4,6-8 However, orbital Doppler ultrasonography is a user-dependent and time-consuming imaging method, in which complete patient cooperation is essential. In addition, these studies reported quite small number of patients with short-term observation after surgery. Recently, a semiautomated system was developed to measure retinal vessel diameters in vivo noninvasively, with good reliability and repeatability.9 Population-based studies using the semiautomated system have shown that retinal vascular diameter changes may be associated with clinical hypertension,10 coronary artery disease,11 and stroke.12 The current
ACCEPTED MANUSCRIPT study used this computer-assisted quantitative assessment software to evaluate the retinal vascular diameter changes before and 1 day after strabismus surgery with the aim of analyzing potential hemodynamic changes that may occur in retinal circulation after strabismus surgery.
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Subjects and Methods
The Medical Ethics Committee of Beijing Tongren Hospital approved the study protocol, and written informed consent was obtained from all the patients. A total of 156 consecutive
SC
patients with horizontal strabismus who underwent rectus muscle surgery between January 2014 and August 2015 at Beijing Tongren Eye Center were enrolled prospectively. The
M AN U
diagnosis of strabismus was made by an experienced surgeon (JF) after detailed examination. Color fundus photographs were taken preoperatively and 1 day after surgery. Slit-lamp examination focused on signs of anterior segment ischemia, characterized by pupillary dilation and distortion, iris atrophy, lens opacities, and hypotonia.7 Patients were divided into
TE D
different groups based on which rectus muscle was transected. Patients were excluded if they had undergone previous anterior or posterior ocular surgery, had systematic diseases (such as diabetes mellitus, systemic hypertension, or any other known vascular diseases), or had
EP
vertical strabismus that required surgery on oblique muscles. Recession and resection were performed using the standard method and involved
AC C
transecting the anterior ciliary arteries. All surgical interventions were performed under general anesthesia by the same experienced surgeon (JF). A limbal conjunctival incision was used in all patients. Following reattachment of the rectus muscle, the conjunctiva was sutured with 6-0 absorbable sutures. Color fundus photographs (45°) of each eye were taken using the CR6-45NM fundus camera (Canon Inc, Japan, Tokyo) centered on the optic disk (Diabetic Retinopathy Study standard field 1) and macula (Diabetic Retinopathy Study standard field 2) before and 1 day after strabismus surgery.13
ACCEPTED MANUSCRIPT To assess retinal vascular caliber changes, the retinal vessel diameters were measured using computer-assisted quantitative assessment software (IVAN; University of Wisconsin, Madison, WI), as described and applied in previous population-based studies.9,10 Average retinal arteriolar or venular width was calculated by means of the Parr-Hubbard formula as
RI PT
the central retinal arteriolar equivalent (CRAE) or central retinal venular equivalent (CRVE). The arteriovenous ratio (AVR) was calculated as CRAE divided by CRVE.14,15 Statistical Analysis
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Statistical analysis was performed using SPSS for Windows, version 22.0 (IBM-SPSS,
Chicago, IL). In a first step, we determined the mean values (with standard deviation) and
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median values of the main outcome parameters. In a second step, we performed paired-samples t test analyses to evaluate the changes of the CRAE, CRVE, and the AVR before and 1 day after the strabismus surgery. A P value of <0.05 was considered significant. Results
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Of the 156 consecutive patients, 8 patients were excluded because of poor-quality pre- or postoperative fundus photographs. The poor quality was due to lack of cooperation in 6 patients and persistent ointment after surgery in 2 patients. A total of 217 eyes of 148 patients
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(74 males [50%]) were included in the analysis. Mean subject age was 13.33 ± 9.52 years (range, 3-51years). Strabismus surgery was performed for exotropia in = 112 cases and
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esotropia in36 cases.
In all 217 no sign of anterior segment ischemia (such as iritis, pupil distortion,
keratitis, irregularity of descemet’s memebrane, posterior synechiae, corneal or iridial neovascularization, rubeosis, cataract, or hypotonia) was found pre- or postoperatively. The mean CRAE at postoperative day 1 was significantly larger than preoperative value (130.64 ± 28.57 vs 124.77 ± 27.21 [P = 0.01]). The mean CRVE at postoperative day 1 did not differ significantly from the preoperative value (174.50 ± 35.35 vs 172.29 ± 31.73 [P = 0.427]). The AVR at postoperative day 1 was significantly larger than preoperative value (0.75 ± 0.09 vs
ACCEPTED MANUSCRIPT 0.73 ± 0.11 [P = 0.003]). See Table 1. We also analyzed the 79 unoperated fellow eyes for comparison and found no clinically significant changes postoperatively no significant difference before surgery and at day 1 after surgery in terms of CRAE (128.97 ± 28.06 vs 132.63 ± 25.86 [P = 0.31]), CRVE
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(173.75 ± 32.80 vs 175.23 ± 32.23 [P = 0.75]), or AVR (0.75 ± 0.10 vs 0.76 ± 0.01 [P = 0.16]).
Of the 217 eyes, 117 eyes (53.9%) underwent surgery with only one rectus muscle
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recession. The other 100 eyes underwent both medial and lateral rectus surgery. For both these groups, significant increase of CRAE and AVR was found. However, further subgroup
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analysis for one rectus surgery group showed significant increase of CRAE and AVR only in the medial rectus recession but not in the lateral rectus recession group. Detailed results of the changes of the retinal vascular caliber before and after surgery are provided in Table 2. Discussion
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Computer-assisted quantitative assessment software (IVAN; University of Wisconsin, Madison, WI) has been used to measure the retinal vascular caliber to evaluate the blood flow and the hemodynamic alterations related to certain ophthalmologic and orbital diseases for
EP
more than 10 years with great reliability and repeatability.9 This noninvasive imaging method has also been used to demonstrate the potential hemodynamic changes of systemic diseases
AC C
such as hypertension, stroke, and diabetes, with conflicting results. In the current study, we used this noninvasive imaging method to analyze the potential effects of strabismus surgery on retinal circulation. Our study analyzed the retinal vascular diameter changes before and 1 day after strabismus surgery in a large series of strabismus patients, with a mean age of 13.07 years. Anterior segment ischemia is a rare but serious complication of strabismus surgery, with a reported incidence of 1/13,000.16-18 In our study there were no signs of anterior segment ischemia pre- or postoperatively.
ACCEPTED MANUSCRIPT As we hypothesized, after the recession or resection of rectus muscles, some hemodynamic changes in retinal circulation may occur because of increased blood flow demands of the anterior segment.4-6 Our study showed that 1 day after surgery CRAE significantly increased compared to the preoperative value (P = 0.01), as did the
RI PT
arteriovenous ratio (P = 0.003). These results suggest that strabismus surgeons should consider retinal circulation status when planning strabismus surgeries, particularly for
patients at risk of retinal vascular diseases, such as diabetic patients. There was no significant
SC
change of the retinal venular diameter (CRVE, P = 0. 43). This result is consistent with a study by Lee and colleagues19 that showed that surgery on two horizontal rectus muscles
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increased ophthalmic artery blood flow during the early postoperative period (1 day) but returned to normal at day 7 or later, as measured by color Doppler imaging. Bayramlar and colleagues4 revealed that color Doppler ultrasound measurements did not show significant change in ophthalmic artery at 1 week and 1 month after surgery on two horizontal rectus
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muscles. But they did not measure the blood flow 1 day after surgery. Retinal venular diameters have been reported to be less sensitive for the retinal blood flow changes,3,6 which may be related to the role of autoregulation played by the retinal
EP
capillary and explain the unchanged CRVE in the present study. Further studies dealing with the late stage of retinal vascular changes are indicated.
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Our study also found that when classified into two groups according to rectus muscles, significant increase of CRAE and AVR was only found in medial rectus recession but not in lateral rectus recession. This is likely due to the fact that the medial rectus and both vertical rectus muscles typically carry two anterior ciliary arteries, whereas the lateral rectus muscle carries only one. This result suggests that at least two anterior ciliary arteries injuries are needed to cause changes in retinal blood flow, and the lateral rectus muscle cut off played a minor role in postoperative change in retina blood flow. There are potential limitations to the generalizability of our results. First, referral bias
ACCEPTED MANUSCRIPT cannot be ruled out. Second, the retinal vascular diameters were assessed on routinely taken fundus photographs, which may lead overlooking of the systolic or diastolic effect on retinal vascular diameter. In conclusion, our results showed that strabismus surgery on horizontal rectus muscles
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may increase retinal blood flow during the early postoperative period. We also found that, surgery on the lateral rectus muscle played a minor role on postoperative retinal blood flow, because it carries only one anterior ciliary artery. Further studies would be needed to analyze
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hemodynamics of vertical rectus muscle transection.
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Preoperative Postoperative t P value
CRAE 124.77 ± 27.28 130.64 ± 28.57 −2.517 0.013
CRVE AVR 172.29 ± 31.73 0.73 ± 0.11 174.50 ± 35.35 0.75 ± 0.09 −0.796 −3.016 0.427 0.003
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AVR, arteriovenous ratio; CRAE, central retinal arteriolar equivalent; CRVE, central retinal venular equivalent.
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Table 1. Characteristics and comparison of retinal vessels caliber before and after surgery of all 217 eyes
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Table 2. Comparison of retinal vessels caliber preoperative and postoperative for eyes with one rectus muscle recession
LR recess (n = 87)
CRAE 123.88 ± 24.58 130.05 ± 27.49 −2.089 0.039 124.73 ± 22.99 136.32 ± 31.77 −1.842 0.036 123.59 ± 25.23 127.89 ± 25.70 −1.293 0.199
CRVE 170.90 ± 29.95 172.15 ± 33.84 −0.363 0.718 173.25 ± 30.10 180.29 ± 39.04 −0.854 0.400 170.10 ± 30.03 169.34 ± 31.62 0.208 0.836
AVR 0.73 ± 0.10 0.76 ± 0.09 −2.915 0.004 0.72 ± 0.08 0.76 ± 0.09 −2.661 0.013 0.73 ± 0.11 0.76 ± 0.09 −2.146 0.035
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MR recess (n = 30)
Time Preoperative Postoperative t P value Preoperative Postoperative t P value Preoperative Postoperative t P value
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Surgical method One rectus muscle recess (n = 117)
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AVR, arteriovenous ratio; CRAE, central retinal arteriolar equivalent; CRVE, central retinal venular equivalent; LR, lateral rectus muscle; MR, medial rectus muscle; Recess, recession.