A New Approach to a Difficult Problem

Research

Original Investigation Restoration of Corneal Sensation With Regional Nerve Transfers and Nerve Grafts A New Approach to a Difficult Problem

Uri Elbaz, MD; Robert Bains, MBChB, FRCS(Plast); Ronald M. Zuker, MD, FRCSC; Gregory H. Borschel, MD; Asim Ali, MD, FRCSC

CME Quiz at IMPORTANCE Corneal anesthesia is recalcitrant to conventional treatment and can lead to jamanetworkcme.com and permanent visual loss. CME Questions 1388

OBJECTIVE To assess the outcomes of a novel sensory reconstructive technique for the treatment of corneal anesthesia.

DESIGN, SETTING, AND PARTICIPANTS This prospective study evaluating a new technique was conducted at a tertiary referral center. Four eyes in 3 patients with corneal anesthesia underwent nerve transfers with nerve grafting to restore corneal sensation. Corneal sensory reconstruction was performed using a segment of the medial cutaneous branch of the sural nerve. Two patients with unilateral trigeminal nerve anesthesia—one following basal skull fracture and another following large posterior fossa tumor resection—underwent corneal sensory reconstruction using the contralateral supratrochlear nerve as the donor sensory nerve. One patient with a history of cerebellar hypoplasia and bilateral congenital corneal anesthesia underwent bilateral corneal sensory reconstruction using the respective ipsilateral supratrochlear nerves as the sensory donor nerves. Corneal anesthesia was evaluated preoperatively and postoperatively in the center of the cornea and in 4 corneal quadrants using a Cochet-Bonnet esthesiometer (Luneau). Complications of the procedure were also documented.

MAIN OUTCOMES AND MEASURES Esthesiometry scores.

RESULTS All eyes had prior complications of corneal anesthesia and had no measurable corneal sensation in the affected eye(s) preoperatively. Two patients—one with cerebellar hypoplasia and the other with posterior fossa tumor resection—had markedly improved corneal sensation 6 months postsurgery (3 eyes; mean [SD] central esthesiometry, 55 [5] mm). A third patient with a history of basal skull fracture underwent unilateral corneal neurotization and recovered 15-mm esthesiometry score centrally after 7.5 months of follow-up. None of the operated on eyes have developed corneal anesthesia–related complications since reconstruction.

CONCLUSIONS AND RELEVANCE Corneal sensory reconstruction provides corneal sensation in previously anesthetic corneas. This can be achieved with minimal morbidity using sural nerve

grafts, which surgeons commonly use to reconstruct nerve gaps elsewhere. This Author Affiliations: Department of multidisciplinary approach restores an ocular defense mechanism and may enable Ophthalmology and Vision Sciences, subsequent corneal transplant in these patients. Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada (Elbaz, Ali); Division of Plastic and Reconstructive Surgery, Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada (Bains, Zuker, Borschel). Corresponding Author: Asim Ali, MD, FRCSC, Department of Ophthalmology and Vision Sciences, Hospital for Sick Children, University of Toronto, 555 University Ave, JAMA Ophthalmol. 2014;132(11):1289-1295. doi:10.1001/jamaophthalmol.2014.2316 Toronto, ON M5G 1X8, Canada Published online July 10, 2014. ([email protected]).

1289

Downloaded From: https://jamanetwork.com/ on 10/01/2021 Research Original Investigation Restoration of Corneal Sensation

he insensate cornea represents a difficult problem that has defied definitive management. Corneal sensation Methods T is critical in maintaining epithelial integrity1 and limbal stem cell function.2 Reduced corneal sensation renders This study was approved by the Research Ethics Board of the the corneal surface prone to injury and decreased reflex tear- Hospital for Sick Children, Toronto, Ontario, Canada, and ing. In addition, the poor healing3 secondary to corneal sen- written informed consent was obtained from patients and/or sory denervation favors the formation of nonhealing epithe- parents/guardians. We included in the study 4 eyes of 3 con- lial defects that ulcerate and perforate if not appropriately secutive patients who had undergone corneal neurotization treated. surgery using a nerve graft. A surgical recommendation was Corneal anesthesia can be categorized into acquired or rendered after mapping patients’ sensation over the face to congenital causes. Its acquired form arises from infectious, ensure sensation in the territory of the donor supratrochlear inflammatory, traumatic, neoplastic, and iatrogenic causes, nerve. The primary outcome measure was the degree of cor- all of which impair the function of the ophthalmic division of neal sensation following surgery. Corneal anesthesia was the trigeminal nerve and lead to neurotrophic keratopathy. evaluated preoperatively and postsurgical intervention cen- The congenital form of this condition may be either isolated trally and in 4 quadrants using a Cochet-Bonnet esthesiom- or syndromic.4-6 Furthermore, corneal anesthesia can be eter (Luneau).16 Corneal sensation of 60 mm was considered either confined to the ophthalmic nerve or alternatively asso- normal. ciated with other ocular conditions, such as strabismus, lag- Two patients underwent unilateral corneal neurotization ophthalmos, or paralytic ectropion, depending on the etiol- and 1 patient underwent bilateral corneal neurotization. All sur- ogy and the extent of involvement of other cranial nerves. gical procedures were performed under general anesthesia. Children may experience photophobia and decreased vision Harvesting of the median cutaneous branch of the sural nerve without pain or distress. Signs may vary from mild conjuncti- and dissection of the donor supratrochlear nerve were car- val injection to sight-threatening conditions, such as corneal ried out simultaneously. The sural nerve was harvested proxi- ulceration or perforation, especially if the facial nerve is mal to distal using a nerve harvesting device (Figure 1A).17 The affected. Unfortunately, few treatment options preserve nerve harvesting device was placed around the nerve and vision. Initial management seeks to maintain the integrity of passed distally to free the nerve from surrounding tissues. The the ocular surface. In cases where a nonhealing corneal epi- nerve was then divided, yielding approximately 10 to 15 cm thelial defect is present, a tarsorrhaphy is mandatory. Ulti- of nerve graft (Figure 1B). The peroneal component of the nerve mately, in the event of corneal perforation, cyanoacrylate was preserved but could be used through separate incisions, gluing or tectonic corneal transplantation are required. How- if required. ever, because of the lack of sensation and the resultant sub- The supratrochlear nerve was found on the surface of the stantial reduction in corneolimbal stem/progenitor cells,2 corrugator supercilii muscle passing cephalad from the supra- grafted corneas do not heal well and therefore graft longevity trochlear notch. This was accessed through a transverse inci- is limited with poor visual prognosis. sion over the medial upper eyelid just inferior to the brow, deep Neurotization involves the transfer of a healthy donor to the origin of the frontalis (Figure 1C and D). An epineural nerve segment into a tissue to reestablish either motor7,8 or window was then created in the side for end-to-side coapta- sensory9,10 innervation. Neurotization is a well-established tion of the sural nerve graft. End-to-side coaptation was our modality of treatment for different clinical conditions9-14 and preferred option to maximally preserve forehead sensation; the technique continues to evolve and gain popularity.7,8 however, in the bilateral case, the supratrochlear nerves were Direct neurotization of the anesthetic cornea was previously found to be small so we divided the nerve distally and per- reported by Terzis et al15 in adults with unilateral facial formed the coaptation end to end. In unilateral cases, the op- paralysis and corneal anesthesia. The technique involved posite supratrochlear nerve was used, necessitating subcuta- the transfer of the contralateral supraorbital and supratroch- neous tunneling of the nerve graft over the nasal bridge lear nerves to the limbal area of the anesthetic cornea. (Figure 1E). Although successful in restoring sensation to the cornea, this The distal nerve graft was reversed and tunneled subcon- approach denervates the contralateral forehead and scalp, junctivally to the perilimbal area of the cornea using a medium- requires a large bicoronal incision with subsequent scarring, sized eyelet Wright needle (Figure 1F). Distally, the epineu- and is not applicable in bilateral palsies wherein all branches rium was removed and the individual fascicles were separated of the ophthalmic division of the trigeminal nerve are (Figure 1G). The fascicles were then placed around the entire affected. limbal circumference to reinnervate all 4 quadrants (Figure 1H The purpose of this study was to report early outcomes shows the separated fascicles prior to tunneling under the con- following a novel corneal neurotization technique in young junctiva; Figure 1I) and secured to the sclera with 10-0 nylon patients. To our knowledge, this is the first report of restora- sutures (Figure 1J). Proximally, coaptation of the graft to the tion of corneal sensation using a sural nerve graft in unilat- cut surface of the supratrochlear nerve was performed under eral and bilateral anesthetic corneas. This novel method rein- the operating microscope with 10-0 nylon sutures and fibrin nervates the cornea, avoids the cosmetically objectionable glue (Tisseel; Figure 1K). The conjunctiva was closed (Figure 1L) bicoronal scar, and is more versatile than the previous bicoro- and lateral tarsorrhaphy was performed in all eyes to opti- nal approach. mize the ocular surface.

1290 JAMA Ophthalmology November 2014 Volume 132, Number 11 jamaophthalmology.com

Downloaded From: https://jamanetwork.com/ on 10/01/2021 Restoration of Corneal Sensation Original Investigation Research

Figure 1. Details of the Surgical Procedure

A B C D

Nerve-harvesting Supratrochlear Nerve-donor nerve device segment

E F Distal G H Proximal and distal donor donor nerves Wright nerve needle

Affected eye

I J K L Supratrochlear nerve Scleral suturing of Subconjunctival nerve tunneling fascicle

Nerve Proximal fascicle donor nerve

A segment of sural nerve is harvested (A and B). A 2-cm upper-lid incision is distributed around the limbus (H), tunneled under the conjunctiva (I), and made inferior to the nasal portion of the brow (C) to locate and isolate the sutured to the sclera using 10-0 nylon sutures (J). K, The proximal end of the supratrochlear nerve (D). E, The nerve graft is tunneled subcutaneously over nerve graft is coapted to the side of the supratrochlear nerve using fibrin glue the nasal bridge in contralateral recipient cases. F, The graft is introduced into and 10-0 nylon suture. At the end of the surgery, the conjunctiva is closed (L) the superior fornix with the aid of a Wright needle. G, The distal end of the and lateral tarsorrhaphy is performed (not shown). nerve graft is separated into its component fascicles. The nerve fascicles are

except for a small paracentral opacity from a resolved chronic Results epithelial defect. The right cornea eventually perforated and a penetrating keratoplasty was carried out at the age of 19 Preoperatively, all eyes had complications of anesthetic cor- months. This graft failed and the patient underwent a second nea including corneal perforation and/or significant scarring transplant that also failed and opacified. Sensory mapping from previous infectious keratitis. No eyes had detectable indicated that sensation was intact in the forehead region corneal sensation preoperatively. Figure 2 shows the time bilaterally. At age 9 years, he underwent bilateral corneal progression of the esthesiometry measurements. Postopera- neurotization using the supratrochlear nerve and sural nerve tively, no ocular complications were reported and, in par- grafts. He developed corneal sensation in his right and left ticular, none of the operated on eyes developed complica- eyes as depicted in Figure 2A and Figure 2B, respectively, tions related to corneal anesthesia during the postoperative within 6 months. follow-up. Patient 2 Patient 1 A girl was referred to our clinic for a preoperative assessment A boy with cerebellar hypoplasia presented to our clinic at 14 prior to excision of a large posterior fossa clear cell menin- months of age with a right corneal ulcer. Bilateral facial gioma at age 10 years. Her sensation was diminished in the nerve paralysis with hearing loss and bilateral corneal anes- distribution of the left trigeminal nerve including reduced thesia were noted. The right eye had poor lid closure and corneal sensation. Her eye examination findings were other- there was a large central corneal ulcer with neovasculariza- wise unremarkable. A week following her meningioma tion, cataract, and esotropia. The left eye was unremarkable resection, she presented with a large central neurotrophic

jamaophthalmology.com JAMA Ophthalmology November 2014 Volume 132, Number 11 1291

Downloaded From: https://jamanetwork.com/ on 10/01/2021 Research Original Investigation Restoration of Corneal Sensation

Figure 2. Cochet-Bonnet Esthesiometry Progression

A 0 15 30 60

000 1515 20 2530 30 6060 60

1-10

0 5 20 60 11-20 21-30

B 31-40 0 0 35 50 41-50 51-60

000 500 3535 35 5555 55

0 0 35 55

Preoperatively POD 63 POD 91 POD 169

C 0 <5 20 50 60

000 5-10<5 <5 2520 10 5050 50 6060 60

0 <5 10 50 60

Preoperatively POD 89 POD 131 POD 194 POD 255

D 0 <5 5 5 15

000 <5<5 <5 <5<5 <5 <5<5 <5 1515 15

0 <5 <5 <5 10

Preoperatively POD 81 POD 130 POD 165 POD 226

Measured in millimeters, centrally, and in 4 corneal quadrant precorneal tumor resection. D, The right eye of patient 3 with corneal anesthesia from basal neurotization and postcorneal neurotization. The right eye (A) and left eye (B) skull fracture. The ranges on the right indicate the levels of corneal sensation in of patient 1 with bilateral corneal anesthesia from cerebellar hypoplasia. C, The millimeters. POD indicates postoperative day. left eye of patient 2 with corneal anesthesia from previous posterior fossa

corneal ulcer in the left eye that decreased her visual acuity Patient 3 to counting fingers at 0.3 m. There was no corneal sensation A 9-year-old boy sustained a basal skull fracture resulting in in the left eye. This ulcer was recalcitrant to treatment and right trigeminal, abducens, and facial nerve palsies. He first her cornea eventually developed deep central scarring. At presented to our clinic at the age of 11 years with infectious age 16 years, she underwent left corneal neurotization using keratitis and corneal anesthesia in his right eye. The exami- the contralateral supratrochlear nerve with sural nerve graft- nation findings of the left eye were unremarkable. Despite all ing. Additional sural nerve graft segments were used to rein- treatments, his cornea perforated, requiring a tectonic cor- nervate her cheek and lips by placing grafts from the intact neal graft, which eventually failed and scarred. At age 17 right mental and infraorbital nerves into the affected left years, he underwent unilateral corneal neurotization from mental and infraorbital nerves, respectively. She recovered the contralateral supratrochlear nerve. Simultaneously, he corneal sensation as shown in Figure 2C within 8.5 months. underwent further sensory reconstruction like patient 2, in Three months after surgery, she said that ipsilateral corneal which sural nerve grafts were used side to end to reconstruct tactile stimulation felt as if the examiner was stroking the the infraorbital and mental nerve defects. In addition, he skin territory of the contralateral supratrochlear nerve just underwent cross-face sural nerve grafting for his facial above the contralateral brow. By 6 months postoperatively, paralysis. The ipsilateral stimuli were first perceived as aris- she said that ipsilateral corneal stimulation no longer elicited ing from the contralateral forehead and after 3 months, as contralateral supratrochlear stimulation, and she instead arising from the ipsilateral cornea in an identical manner to perceived the tactile stimulus as originating from the ipsilat- that seen in patient 2. After 6 months, he recovered protec- eral cornea. tive sensation in all quadrants as shown in Figure 2D.

1292 JAMA Ophthalmology November 2014 Volume 132, Number 11 jamaophthalmology.com

Downloaded From: https://jamanetwork.com/ on 10/01/2021 Restoration of Corneal Sensation Original Investigation Research

Figure 3. Ocular Surface Improvement

A B

Preoperative unstable ocular surface (A) and 9 months postoperative stable ocular surface (B) in patient 2. The patient underwent fine-needle diathermy with intrastromal bevacizumab injection prior to corneal neurotization with no recurrence of corneal vessels 9 months after surgery.

patients who recover corneal sensation following nerve recon- Discussion struction but have vision-limiting corneal scarring, we plan to offer corneal transplantation. Corneal anesthesia requires close monitoring; threatens vi- The previously reported direct corneal neurotization sion; and imposes medical, social, and economic burdens to technique15 is revolutionary but has some shortcomings; we the patient and society. Most treatments do not address the have addressed some of these concerns with this new strat- underlying cause and outcomes in these cases remain poor. egy. It can only be used in unilateral disease where the con- We present a novel technique that restores corneal sensation tralateral supratrochlear and supraorbital nerves have intact in unilateral and bilateral corneal anesthesia using a sural nerve sensation. Moreover, it requires a large bicoronal incision and graft. This approach may be used to maintain ocular surface extensive dissection area to reflect the scalp over the fore- integrity (Figure 3), reduce the risk for infections, and main- head to expose and isolate the entirety of the delicate distal tain vision. It may also enable corneal transplantation in se- ends of the donor nerves. The bicoronal incision leaves a large verely scarred corneas. scar over the top of the head from ear to ear, which can be cos- In unilateral neurotization cases, afferent signals arriv- metically unappealing. ing from the affected side travel to the contralateral healthy Unlike the direct neurotization technique, the sural graft/ trigeminal ganglion and the patient learns to distinguish the transfer approach enables management of bilateral corneal an- stimulus location over time as was demonstrated in patients esthesia. The harvested sural nerve segment is long enough 2 and 3. In the patient with bilateral ophthalmic nerve dam- to permit other nerves to serve as potential sources of inner- age, a different reconstructive strategy was chosen because sen- vation. In these instances, coaptation to branches arising from sation in the distribution of the ipsilateral supratrochlear nerves the maxillary division or even the mandibular division of the was intact. trigeminal nerves are possible as long as their function is nor- In a previous study,15 the contralateral supratrochlear and mal. The grafted sural nerve enables the recipient nerve to ex- supraorbital nerves were directly transferred to provide cor- tend its axons to reach the cornea. This donor nerve usually neal sensation. The average (SD) reported time to reestablish cor- contains 4 to 8 fascicles, each of which may be separated to neal sensibility after direct neurotization was 2.80 (2.17) years cover the entire corneal limbus. in 6 eyes, with average (SD) denervation time of 7.00 (8.56) years. The extent of growth of the axons into the cornea follow- The resulting sensibility was high (≥50 mm) in 1 patient, mod- ing coaptation depends on the time elapsed from surgery, the erate (>20-<50 mm) in 2 patients, low (≤20 mm) in 2 patients, distance to the target organ, and the age of the patient.18 and not available in 1 patient after a mean (SD) of 16 (2.4) years. However, the exact mechanism of corneal reinnervation In some of their patients, corneal scarring resolved and an im- postnerve transfer is not completely understood especially in provement in visual acuity was observed. In our patients, the view of the fact that the distal donor nerve fascicles are laid improvement in corneal sensibility was already noticeable af- around the limbus and not directly coapted to corneal ter 3 months of follow-up in 3 of 4 eyes. It may be that the young nerves. Following peripheral nerve transection, Wallerian population in our study partly accounted for this difference. Our degeneration occurs in the distal transected segment, which approach might also conduct more sensory fibers into the cor- creates a microenvironment for axonal regeneration. Similar nea because we did not rely on the very wispy distal portions processes take place following nerve graft coaptation. Fur- of the supratrochlear and supraorbital nerves; rather, we con- thermore, the ability of regenerating axons to penetrate the nected the nerve graft to the much larger-caliber proximal su- cornea has been demonstrated in several studies following pratrochlear nerve. In our series, we noted no change in visual laser in situ keratomileusis, photorefractive keratectomy, and acuity during the study duration, which is not surprising given penetrating keratoplasty.19-26 Transection of corneal nerves that 2 of the 4 eyes had significant scarring after failed previ- during penetrating keratoplasty occurs in the corneal tissue ous corneal transplants and 1 eye had moderate amblyopia. In itself, after which spontaneous nerve regeneration takes

jamaophthalmology.com JAMA Ophthalmology November 2014 Volume 132, Number 11 1293

Downloaded From: https://jamanetwork.com/ on 10/01/2021 Research Original Investigation Restoration of Corneal Sensation

place. However, despite the short distance, nerve regenera- plications is low28 and therefore justifies the use of the sural tion in corneal transplants is suboptimal because of misalign- nerve in corneal reinnervation. ment of proximal and distal corneal Schwann cell channels,19 The limitation of our study was that corneal reinnerva- which is partly responsible for the reduced corneal sensation tion was only determined clinically. Despite the high correla- after penetrating keratoplasty. Following laser in situ ker- tion demonstrated between functional and morphologic find- atomileusis, which involves transection of superficial stromal ings in neurotrophic keratitis,29 evaluation of morphologic nerves, stromal reinnervation is achieved through the appo- parameters pertinent for monitoring reversal of corneal anes- sition of these channels as demonstrated in a rabbit model.27 thesia, such as an increase in nerve density, decreased den- In contrast, in posttraumatic or iatrogenic corneal anesthesia, sity of hyperreflective keratocytes, or an increase in epithe- the distance from nerve transection site to end organ is usu- lial cell density, would provide anatomical validation of nerve ally significantly larger. Therefore, the Schwann cell tubes regeneration and resumption of sensation in our patients. Fur- that support spontaneous axonal regeneration degenerate ther investigation with in vivo confocal microscopy before and and may atrophy by the time this process takes place. In con- after surgery or corneal histopathologic assessment of cor- genital cases, the neuronal pathway to the cornea has never neal buttons excised from patients undergoing corneal trans- been established. By coapting a fresh nerve graft to the plantation following neurotization surgery could therefore pro- supratrochlear nerve, the new Schwann cells’ basal laminae vide more robust evidence of nerve regeneration. in the donor nerve graft support axonal regeneration. We sur- mised that regenerating axons find their way from the surrounding nerve graft fascicles to the corneal stroma or at Conclusions least to the subepithelial level, thereby restoring sensation. The sural nerve is purely sensory. Its removal results in a Corneal anesthesia poses a challenge to the ophthalmologist numb patch of skin over the anterolateral ankle and does not as conservative treatments are often inadequate and may not interfere with mobility. Postoperative sural nerve-donor site prevent visual loss. Corneal neurotization using a peripheral infection, untoward scarring, and neuropathic pain rarely sensory nerve graft is a promising technique that gives hope occur28 following sural nerve harvest, and none of these com- to patients with this condition and expands our therapeutic plications arose in our patients. The incidence of these com- armamentarium to restore corneal sensation.

ARTICLE INFORMATION REFERENCES 10. Brunelli GA. Sensory nerves transfers. J Hand Submitted for Publication: January 20, 2014; final 1. Garcia-Hirschfeld J, Lopez-Briones LG, Belmonte Surg Br. 2004;29(6):557-562. revision received April 26, 2014; accepted April 29, C. Neurotrophic influences on corneal epithelial 11. Narakas AO, Hentz VR. Neurotization in brachial 2014. cells. Exp Eye Res. 1994;59(5):597-605. plexus injuries: indication and results. Clin Orthop Published Online: July 10, 2014. 2. Ueno H, Ferrari G, Hattori T, et al. Dependence of Relat Res. 1988;(237):43-56. doi:10.1001/jamaophthalmol.2014.2316. corneal stem/progenitor cells on ocular surface 12. Akasaka Y, Hara T, Takahashi M. Restoration of Author Contributions: Drs Elbaz and Ali had full innervation. Invest Ophthalmol Vis Sci. 2012;53(2): elbow flexion and wrist extension in brachial plexus access to all of the data in the study and take 867-872. paralyses by means of free muscle transplantation responsibility for the integrity of the data and the 3. Gallar J, Pozo MA, Rebollo I, Belmonte C. Effects innervated by intercostal nerve. Ann Chir Main accuracy of the data analysis. Senior coauthors Drs of capsaicin on corneal wound healing. Invest Memb Super. 1990;9(5):341-350. Borschel and Ali contributed equally to this work. Ophthalmol Vis Sci. 1990;31(10):1968-1974. 13. Tucker HM. Combined laryngeal framework Study concept and design: Elbaz, Zuker, Borschel, 4. Rosenberg ML. Congenital trigeminal medialization and reinnervation for unilateral vocal Ali. anaesthesia: a review and classification. Brain. fold paralysis. Ann Otol Rhinol Laryngol. 1990;99(10, Acquisition, analysis, or interpretation of data: All 1984;107(pt 4):1073-1082. pt 1):778-781. authors. 5. Ramaesh K, Stokes J, Henry E, Dutton GN, 14. Kunihiro T, Kanzaki J, O-Uchi T. Drafting of the manuscript: Elbaz, Bains, Zuker, Hypoglossal-facial nerve anastomosis: clinical Borschel. Dhillon B. Congenital corneal anesthesia. Surv Ophthalmol. 2007;52(1):50-60. observation. Acta Otolaryngol Suppl. 1991;487: Critical revision of the manuscript for important 80-84. intellectual content: All authors. 6. Mathen MM, Vishnu S, Prajna NV, Vijayalakshmi Statistical analysis: Elbaz. P, Srinivasan M. Congenital corneal anesthesia: 15. Terzis JK, Dryer MM, Bodner BI. Corneal Obtained funding: Ali. a series of four case reports. Cornea. 2001;20(2): neurotization: a novel solution to neurotrophic Administrative, technical, or material support: Elbaz, 194-196. keratopathy. Plast Reconstr Surg. 2009;123(1): 112-120. Bains, Zuker, Borschel. 7. Hontanilla B, Marre D, Cabello A. Cross-face Study supervision: Zuker, Borschel, Ali. nerve grafting for reanimation of incomplete facial 16. Cochet P, Bonnet R. Corneal esthesiometry: Conflict of Interest Disclosures: All authors have paralysis: quantitative outcomes using the FACIAL performance and practical importance [in French]. completed and submitted the ICMJE Form for CLIMA system and patient satisfaction. J Reconstr Bull Soc Ophtalmol Fr. 1961;6:541-550. Disclosure of Potential Conflicts of Interest and Microsurg. 2014;30(1):25-30. 17. Fattah A, Borschel GH, Zuker RM. none were reported. 8. Flores LP, Martins RS, Siqueira MG. Clinical Reconstruction of facial nerve injuries in children. Additional Contributions: We thank medical results of transferring a motor branch of the tibial J Craniofac Surg. 2011;22(3):782-788. imaging specialists Cynthia VandenHoven, BAA, nerve to the deep peroneal nerve for treatment of 18. Höke A. Mechanisms of disease: what factors CRA, and Leslie MacKeen, BSc, CRA, from the foot drop. Neurosurgery. 2013;73(4):609-615; limit the success of peripheral nerve regeneration in Department of Ophthalmology and Vision Sciences, discussion 615-616. humans? Nat Clin Pract Neurol. 2006;2(8):448-454. Hospital for Sick Children, University of Toronto, for 9. Gordon L, Buncke HJ. Restoration of sensation 19. Tervo T, Vannas A, Tervo K, Holden BA. all the images presented herein. They did not to the sole of the foot by nerve transfer: a case Histochemical evidence of limited reinnervation of receive compensation for their contributions. report. J Bone Joint Surg Am. 1981;63(5):828-830. human corneal grafts. Acta Ophthalmol (Copenh). 1985;63(2):207-214.

1294 JAMA Ophthalmology November 2014 Volume 132, Number 11 jamaophthalmology.com

Downloaded From: https://jamanetwork.com/ on 10/01/2021 Restoration of Corneal Sensation Original Investigation Research

20. Kauffmann T, Bodanowitz S, Hesse L, Kroll P. 3-year longitudinal study. Invest Ophthalmol Vis Sci. prevention and treatment. J Refract Surg. 2008;24 Corneal reinnervation after photorefractive 2004;45(11):3991-3996. (4):396-407. keratectomy and laser in situ keratomileusis: an in 24. Erie JC, McLaren JW, Hodge DO, Bourne WM. 27. Chan-Ling T, Tervo K, Tervo T, Vannas A, Holden vivo study with a confocal videomicroscope. Ger J Recovery of corneal subbasal nerve density after BA, Eranko L. Long-term neural regeneration in the Ophthalmol. 1996;5(6):508-512. PRK and LASIK. Am J Ophthalmol. 2005;140(6): rabbit following 180 degrees limbal incision. Invest 21. Latvala T, Linna T, Tervo T. Corneal nerve 1059-1064. Ophthalmol Vis Sci. 1987;28(12):2083-2088. recovery after photorefractive keratectomy and 25. Sonigo B, Iordanidou V, Chong-Sit D, et al. In 28. Hallgren A, Björkman A, Chemnitz A, Dahlin LB. laser in situ keratomileusis. Int Ophthalmol Clin. vivo corneal confocal microscopy comparison of Subjective outcome related to donor site morbidity 1996;36(4):21-27. intralase femtosecond laser and mechanical after sural nerve graft harvesting: a survey in 41 22. Kohlhaas M. Corneal sensation after cataract microkeratome for laser in situ keratomileusis. patients. BMC Surg. 2013;13(1):39. and refractive surgery. J Cataract Refract Surg. Invest Ophthalmol Vis Sci. 2006;47(7):2803-2811. 29. Lambiase A, Sacchetti M, Mastropasqua A, 1998;24(10):1399-1409. 26. Ambrósio R Jr, Tervo T, Wilson SE. Bonini S. Corneal changes in neurosurgically 23. Calvillo MP, McLaren JW, Hodge DO, Bourne LASIK-associated dry eye and neurotrophic induced neurotrophic keratitis. JAMA Ophthalmol. WM. Corneal reinnervation after LASIK: prospective epitheliopathy: pathophysiology and strategies for 2013;131(12):1547-1553.

OPHTHALMIC IMAGES

Intrathecal Anesthesia After Retrobulbar Block, With Terson-Like Syndrome

Roger A. Goldberg, MD, MBA; Nadia K. Waheed, MD

Spin: –108 A Tilt: 2 B C

Saggital (A) and axial (B) computed tomographic images demonstrate anesthetic injected into the optic nerve during retrobulbar block. Images were obtained while the patient was intubated for apnea that developed approximately 5 minutes after retrobulbar injection. The patient was successfully extubated 6 hours later. One day later, the patient was noted to have retinal hemorrhages consistent with a Terson-like syndrome (C). No afferent pupillary defect was present, and Snellen visual acuity remained 20/25.

jamaophthalmology.com JAMA Ophthalmology November 2014 Volume 132, Number 11 1295

Downloaded From: https://jamanetwork.com/ on 10/01/2021