Laser speckle contrast imaging enables perfusion monitoring of the anterior segment during eye muscle surgery

We demonstrate that laser speckle contrast imaging can be used to monitor blood perfusion noninvasively during the detachment of ocular muscles, which may be a valuable tool for reducing the risk of anterior segment ischemia as a complication of strabismus surgery. We demonstrate that laser speckle contrast imaging can be used to monitor blood perfusion noninvasively during the detachment of ocular muscles, which may be a valuable tool for reducing the risk of anterior segment ischemia as a complication of strabismus surgery. During most strabismus procedures, rectus muscles and their corresponding anterior ciliary arteries are severed. Damage to multiple vessels may result in anterior segment ischemia (ASI), a rare but potentially vision-threatening complication of strabismus surgery. To minimize the risk of ASI, strabismus surgery protocols advocate manipulation of no more than two rectus muscles at a time and one more after a minimum of 6 months’ healing time. However, these recommendations are based on empirical observations of clinical outcome and were developed nearly a century ago. To date, no method has proved successful in monitoring the effects of strabismus surgery on anterior segment circulation in real time. We report our successful use of laser speckle contrast imaging (LSCI) to map blood perfusion to the anterior segment of the eye during extraocular muscle surgery. The technique is noninvasive and has proved useful in monitoring blood perfusion in skin with high spatial and temporal resolution.1Mirdell R. Farnebo S. Sjöberg F. Tesselaar E. Interobserver reliability of laser speckle contrast imaging in the assessment of burns.Burns. 2019; 45: 1325-1335Crossref PubMed Scopus (5) Google Scholar LSCI has previously been used in measurements of perfusion in the retina and in reconstructive surgery.2Ansson C.D. Berggren J.V. Tenland K. et al.Perfusion in upper eyelid flaps: effects of rotation and stretching measured with laser speckle contrast imaging in patients.Ophthalmic Plast Reconstr Surg. 2020; 36: 481-484Crossref PubMed Scopus (5) Google Scholar, 3Berggren J. Castelo N. Tenland K. et al.Reperfusion of free full-thickness skin grafts in periocular reconstructive surgery monitored using laser speckle contrast imaging.Ophthalmic Plast Reconstr Surg. 2021; 37: 324-328Crossref PubMed Scopus (0) Google Scholar, 4Cheng H. Yan Y. Duong T.Q. Temporal statistical analysis of laser speckle images and its application to retinal blood-flow imaging.Opt Express. 2008; 16: 10214-10219Crossref PubMed Scopus (106) Google Scholar A 72-year-old man was referred to the Skåne University Hospital, Lund, for enucleation of the left eye after previous diagnosis and treatment of uveal melanoma. A biopsy had been taken, followed by treatment with iodine plaque radiotherapy. The patient had developed increasing inflammation, resulting in complete retinal detachment and iris bombe. Physicians were unable to monitor his response to treatment, and the patient was referred for enucleation. Presurgical examination revealed discrete postoperative scars on the conjunctiva and visual acuity of hand motion. Apart from the perfusion measurements, enucleation was performed according to standard procedure under general anesthesia. Prior to surgery, the patient gave his informed consent to participate in the study, which had been approved by the Swedish Ethical Review Authority. Perfusion was monitored using LSCI (PeriCam PSI NR, Perimed AB, Järfälla, Sweden). In this procedure, the eye is illuminated by an infrared laser (785 nm wavelength), and the interference of the light backscattered from moving particles creates a speckle pattern that may be interpreted as perfusion, given in arbitrary units. Perfusion monitoring was performed during the enucleation procedure, before and after each rectus muscle was cut in the following order: (1) lateral rectus muscle, (2) medial rectus muscle, (3) inferior rectus muscle, and (4) the superior rectus muscle. Finally, (5) the optic nerve with the ophthalmic artery was cut, and measurements were performed after all sources of circulation to the eyeball had been completely removed. The region monitored was the area between two concentric circles, the inner one at the limbus and the outer one 4–5 mm further out, where the anterior ciliary arteries branch off piercing the sclera to go into the eye and form the circularly arranged vessel network of the paralimbal conjunctiva and episclera. The results showed that the ciliary circulation in the anterior segment could be mapped in detail using LSCI. The paralimbal perfusion remained relatively stable until the fourth, final rectus muscle (the superior rectus muscle) was detached, after which a significant decrease in perfusion to approximately 50% was seen. When the optic nerve was cut, and with it the ophthalmic artery, perfusion decreased to almost zero. For detailed results, see Figure 1. Only a few studies have previously evaluated anterior segment circulation in relation to strabismus surgery in humans. These were either conducted with technologies that are not clinically applicable or are invasive, and none of the techniques is suitable for perfusion monitoring during surgery. In 1978, Hayreh and colleagues5Hayreh S.S. Scott W.E. Fluorescein iris angiography II. Disturbances in iris circulation following strabismus operation on the various recti.Arch Ophthalmol. 1978; 96: 1390-1400Crossref PubMed Scopus (69) Google Scholar examined circulation in the iris in 33 blue or green eyes in 31 patients admitted for strabismus surgery preoperatively and within 24 hours postoperatively, using fluorescein angiography. In cases of tenotomy of only horizontal muscles, no difference was seen in the circulation; however, when vertical muscles were detached, a delay in the filling of the vessels was seen postoperatively in the corresponding part of the iris. Other groups have used fluorescein angiography in a similar manner.6Olver J.M. Lee J.P. Recovery of anterior segment circulation after strabismus surgery in adult patients.Ophthalmology. 1992; 99: 305-315Abstract Full Text PDF PubMed Scopus (37) Google Scholar,7Kaeser P.F. Klainguti G. Anterior segment angiography in strabismus surgery.Klin Monbl Augenheilkd. 2012; 229: 362-364Crossref PubMed Scopus (9) Google Scholar In 2001, Chan and colleagues8Chan T.K. Rosenbaum A.L. Rao R. Schwartz S.D. Santiago P. Thayer D. Indocyanine green angiography of the anterior segment in patients undergoing strabismus surgery.Br J Ophthalmol. 2001; 85: 214-218Crossref PubMed Scopus (26) Google Scholar performed pre- and postoperative indocyanine angiography on the anterior segment in patients undergoing strabismus surgery. Most of the patients showed perfusion defects in the early postoperative phase, but almost all recovered within 3-22 weeks after surgery. In comparison with fluorescein, indocyanine angiography has the advantage of being usable in darker irides. Although these methods can provide detailed information on anterior segment circulation, they cannot be used during surgery and are invasive. Optical coherence tomography angiography (OCT-A) has recently been developed. In 2018 Velez and colleagues9Velez F.G. Davila J.P. Diaz A. Corradetti G. Sarraf D. Pineles S.L. Association of change in iris vessel density in optical coherence tomography angiography with anterior segment ischemia after strabismus surgery.JAMA Ophthalmol. 2018; 136: 1041-1045Crossref PubMed Scopus (20) Google Scholar used OCT-A to measure iris vessel density before and after strabismus surgery. Only a small decrease of 2%-3% was observed. Although it is noninvasive, OCT-A only provides static information on iris vessel density and cannot be used to monitor perfusion in real time. There is thus a need for non-invasive, safe perfusion monitoring methods that can be used both pre- and postoperatively as well as intraoperatively. An adequate perfusion monitoring technique could possibly enable the prediction and minimization of the risk of ASI after strabismus surgery. Setting aside surgical tradition, we hypothesize that in many cases it would be possible to operate on three muscles during a single surgical session as well as a fourth muscle after a period of healing. The benefit of studying the effect of extraocular muscle removal on anterior segment circulation using enucleation is that it allows all muscles as well as the optic nerve to be detached in a single surgery, enabling complete mapping of the blood supply to the anterior segment of the eye. However, the anatomy and physiology will differ from that of a healthy eye because of the underlying conditions leading to enucleation, such as tumor, previous treatments, and potential inflammation. Because the vertical rectus muscles contribute more to the perfusion of the anterior segment than the horizontal, the order of detachment may also affect results. The present study shows that LSCI can be used to visualize and quantify the decrease in perfusion that occurs when the rectus muscles of the eye are detached. Although we employed it during an enucleation, the technique is applicable to strabismus surgery as the muscles are detached in a similar way. Our objective is therefore to use this technology during strabismus surgery. To further this research, LSCI must be evaluated in perfusion monitoring in different strabismus surgical procedures in patients with varying risks of anterior ischemia. It would also require postoperative measurements in the days following the surgery, because ASI only becomes symptomatic postoperatively. LSCI has been approved for medical use and employs a class 1 laser that has been declared safe to use in and around the eyes; we are confident that it will be suitable for use in strabismus surgery. It also carries no risk of allergic reactions or anaphylaxis, unlike angiographic methods, and is thus suitable for repeated measurements. In conclusion, LSCI is a promising modality enabling real-time, noninvasive perfusion monitoring of the anterior segment during surgery on the extraocular muscles.