Management of Corneal Scarring Secondary to Herpes Zoster Keratitis

REVIEW

Omar M. Hassan, MD,* Asim V. Farooq, MD,† Ketki Soin, MD,* Ali R. Djalilian, MD,* and Joshua H. Hou, MD‡

erpes zoster ophthalmicus is the reactivated form of Purpose: To review the management of visually significant corneal Hvaricella zoster along the ophthalmic branch of the scarring secondary to herpes zoster keratitis (HZK). trigeminal nerve. Herpes zoster keratitis (HZK) indicates Methods: Literature review. corneal involvement and can affect all layers of the cornea in the form of a pseudodendritic epitheliopathy, stromal kerati- Results: Management options for visually significant corneal tis, or endotheliitis, among other clinical presentations.1 scarring secondary to HZK include scleral contact lenses, photo- Because the causative virus is neurotropic and develops refractive or phototherapeutic keratectomy, lamellar keratoplasty, lifelong latency in humans, it has an ability to cause penetrating keratoplasty, and keratoprosthesis. Many authors progressive damage to corneal sensory nerves through recommend tarsorrhaphy in at-risk patients at the time of corneal multiple reactivation episodes. Resultant severe neurotrophic transplantation. Most published studies either did not mention or keratopathy can lead to decreased aqueous tear production did not use systemic antivirals at the time of surgery. Longer and may limit the delivery of growth factors important for quiescent periods before surgical intervention may be associated corneal epithelial homeostasis.2,3 Therefore, in addition to with increased rates of graft survival. Reports of HZK recurrence causing visually significant corneal scarring, HZK can lead to after live-attenuated vaccine administration suggest that risks and ocular surface instability, persistent epithelial defects, and benefits of the vaccine should be carefully considered. Overall, the stromal melts. Traditional rigid gas-permeable contact lenses prognosis of surgical intervention for corneal scarring due to HZK cause epithelial thinning and desquamation, and their use may relies on appropriate patient selection and measures to ensure not be advisable in severe neurotrophic keratopathy.4 It ocular surface stability. There remains a serious risk of ocular follows that the management of visually significant corneal surface instability and corneal melt in these patients. Unfortu- scarring related to HZK must take into consideration the nately, there is a lack of prospective studies in this area to guide presence of active ocular surface disease and/or inflammation clinical management. with concurrent neurotrophic changes. In this study, we review the present literature regarding the management of fi Conclusions: Patients with visually signi cant corneal scarring corneal scarring in HZK. secondarytoHZKmayhavegoodoutcomeswiththeappropriate medical and surgical considerations, particularly in the absence of active ocular surface disease and inflammation. Those with active disease may METHODS benefit from delaying surgical intervention until a satisfactory quiescent A review of the English language literature on the period has been achieved. Prospective studies, such as the proposed management of corneal scarring in patients with a history of Zoster Eye Disease Study, are imperative for validating these principles HZK was performed on PubMed. Search terms included and determining evidence-based management guidelines. “herpes zoster keratitis,”“herpes zoster keratitis scleral lens,” and “herpes zoster ophthalmicus management” without a set Key Words: Herpes Zoster, Zoster Keratitis, Corneal Scarring period. Case reports describing only management of active (Cornea 2017;36:1018–1023) keratitis or corneal melt were excluded. Case series that included both cases of active keratitis or corneal melt and cases of isolated corneal scarring were included, although the cases of active keratitis and melt were excluded from our analysis.

Received for publication January 6, 2017; revision received March 17, 2017; accepted March 26, 2017. Published online ahead of print June 2, 2017. Scleral Contact Lenses From the *Department of Ophthalmology and Visual Sciences, University of Refractive correction of patients with corneal scarring Illinois Eye and Ear Inﬁrmary, Chicago, IL; †Department of Ophthalmol- ogy and Visual Science, University of Chicago, Chicago, IL; and from HZK can be challenging. Irregular astigmatism from ‡Department of Ophthalmology and Visual Neurosciences, University of scarring may not be amenable to correction by standard rigid Minnesota, Minneapolis, MN. gas-permeable lenses because of the increased risk for lens- The authors have no funding or conﬂicts of interest to disclose. related complications in the setting of severe neurotrophic Reprints: Joshua H. Hou, MD, Department of Ophthalmology and Visual Neurosciences, University of Minnesota, 420 Delaware St SE, MMC 493, keratopathy; they may be considered for patients with para- Minneapolis, MN 55455 (e-mail: [email protected]). central scarring and mildly decreased or normal corneal Copyright © 2017 Wolters Kluwer Health, Inc. All rights reserved. sensation. Scleral contact lenses address irregular astigmatism

1018 | www.corneajrnl.com Cornea Volume 36, Number 8, August 2017

Copyright Ó 2017 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. Cornea Volume 36, Number 8, August 2017 Management of Corneal Scarring Secondary to HZK while also creating a fluid reservoir between the device and epithelial defect with a scleral lens in the setting of previous cornea. Their use has been well-described in the management HZK has also been described.8 These reports suggest that of neurotrophic keratopathy and severe ocular surface scleral contact lenses may be considered for visual and ocular disease.5–10 There have been at least 2 cases series of patients surface rehabilitation in patients with a history of corneal with severe ocular surface disease treated with scleral contact scarring due to HZK. lenses specifically including patients with a history of HZK.9,10 These studies demonstrated that cohorts including patients with HZK show good ocular surface stability and Phototherapeutic/Photorefractive Keratectomy improvement in best-corrected visual acuity (BCVA) with Surgical intervention may be considered for patients scleral contact lenses. Successful treatment of a persistent with visually significant corneal scarring not correctable with

TABLE 1. Outcomes of Keratoplasty in Herpes Zoster Keratitis Author Kosker et al Marsh and Cooper Soong et al Tanure et al Reed et al Hedges Study type Retrospective chart Retrospective chart Retrospective chart Retrospective chart Retrospective chart Retrospective chart review review review review review review with histopathology Cases 9 PKP, 1 DALK 6 PKP, 1 DALK 9 PKP 14 PKP 7 PKP 2 PKP Active ocular NA None None None None 1 surface disease Preoperative 85 (range: 0–348 mo) NA 39 mo 10.1 yrs 35.6 mo in NA quiescent noninflamed eyes waiting period (mean) Topical steroids Prednisolone acetate NA Prednisolone acetate Prednisolone acetate Yes (not specified) NA 1% 1% 1% Topical steroid every 4 to 6 hours NA TID, but up to every 2 every 4–6 hours NA NA dosing if used hours for PKP w/CE Systemic None NA None None NA NA antivirals Antiviral dosing None NA None None NA NA if used Previous surgery/ 1 PKP w/previous 1 CE, 3 argon laser NA, but no previous 1 PKP, 2 argon laser 1 corneal patch graft 1 CE procedures conjunctival flap PKP Concurrent 7 CE 2 CE 4 CE 5 tarsorrhaphy 5 tarsorrhaphy NA surgery 4 PKP w/tarsorrhaphy 2 anterior vitrectomy 3 CE 3 CE 1 DALK w/tarsorrhaphy Range of HM in 7, LP in 1; NA 20/60 to CF 20/70 to LP 20/200 to LP NA preoperative 2.36 6 0.89, mean VA 20/4580 Range of 1.00 6 1.03, mean 6/9–6/24 20/20 to CF 20/25 to CF 20/25 to LP (20/25– NA postoperative 20/200 20/400 in surviving VA grafts) Postoperative 12–132 mo 24–108 mo 5–40 mo (mean 18) 16–110 mo (mean 50) 7–30 mo NA follow-up Graft rejection 312810 Graft failures None 12511 Author Ocular surface Consider preoperative Consider PKP when Recommend frequent PKP can be PKP can be conclusions/ disease and shorter argon laser for long quiescent follow-up, performed for successful once comments quiescent period vascularized period, no ocular preservative-free visual inflammation may increase corneas surface disease, lubricants, and rehabilitation alone resolves rejection risk and controlled IOP topical steroids Consider tarsorrhaphy Consider tarsorrhaphy Tarsorrhaphy is at the time of PKP for ocular surface important to protect for ocular surface stability the ocular surface stability in cases of neurotrophic keratopathy

CE, cataract extraction; CF, counting ﬁngers; DALK, deep anterior lamellar keratoplasty; HM, hand motions; LP, light perception; NA, not reported; VA, visual acuity.

Copyright Ó 2017 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. Hassan et al Cornea Volume 36, Number 8, August 2017 a scleral contact lens, or who are otherwise poor candidates. a follow-up of 38 months, the graft was clear and BSCVA was However, any ocular surface procedure in the setting of 20/60. Postoperative complications in this patient included neurotrophic keratopathy must take into account the risk of severe dry eye and detachment of Descemet membrane.14 postoperative persistent corneal epithelial defect and melt. Marsh et al retrospectively reviewed 9 patients with HZK who Neurotrophic keratopathy develops in approximately 12.8% underwent corneal transplantation, one of whom underwent of HZK cases, and patients with unilateral HZK can develop lamellar keratoplasty for disciform scarring and lipid keratop- bilateral changes in corneal nerve morphology.11,12 athy. At last follow-up of 2 years after surgery, the lamellar One case described the use of phototherapeutic kera- graft was noted to be clear.15 tectomy (PTK) with mitomycin C, followed by photorefractive keratectomy (PRK) in the same eye of a 20-year-old man.13 The patient had a central stromal scar at a depth of Penetrating Keratoplasty 250 mm as measured by confocal microscopy. Of note, There have been several case reports and case series preoperatively there was no significant ocular surface disease, describing penetrating keratoplasty (PKP) in the manage- and although the preoperative BCVA was 20/25, the patient ment of corneal scarring secondary to HZK (Table 1). Soong complained of significant glare. Corneal sensation was noted et al retrospectively reviewed 9 cases at the University of to be intact. Two fine fronds of neovascularization near the Michigan. Patient ages ranged from 55 to 86 years. Three limbus were treated with the argon laser and 1% topical patients had PKP alone, 4 had concurrent cataract extraction prednisolone acetate 2 weeks before PTK. The patient had an with posterior chamber intraocular lens placement, and 2 uncorrected visual acuity of 20/25 in the surgical eye had PKP with anterior vitrectomy. None of the patients had postoperatively with resolution of glare symptoms. active ocular surface disease, elevated intraocular pressure, or active uveitis at the time of surgery. Seven of 9 patients had a clear graft at last follow-up. The average quiescent Lamellar Keratoplasty period before surgery was 39 months. The 2 patients who There are 2 reported cases describing the use of anterior had graft failure had the shortest quiescent intervals (4 and lamellar keratoplasty in HZK. The results of these cases are 11 months).16 Tanure et al noted in another series that summarized along with the outcomes of other types of permanent tarsorrhaphy was performed in patients with corneal transplantation surgery for HZK in Table 1. We did clinically significant neurotrophic keratopathy.17 Findings not find any reports in the literature specifically describing from the remaining studies in this category are summarized endothelial keratoplasty performed for HZK-related in Table 1.17–19 endothelial decompensation. Kosker et al performed 1 deep anterior lamellar keratoplasty with concurrent tarsorrhaphy in a 55-year-old patient Keratoprosthesis with a quiescent period of 348 months. Initial preoperative best There is 1 case report and 1 case series describing the uncorrected visual acuity (BSCVA) was light perception. After Boston keratoprosthesis in the management of corneal

TABLE 2. Boston Keratoprosthesis for the Management of Corneal Scarring Secondary to Herpes Zoster Keratitis Author Todani et al Brown et al Study Retrospective chart review Retrospective chart review Cases 74-year-old woman from CF to 20/25 w/Kpro 4 Boston keratoprosthesis for HZK Active ocular surface disease NA NA Preoperative quiescent waiting period NA NA Topical steroids NA Prednisolone acetate 1.0% Topical steroid dosing if used NA QID tapered every 3 mo Systemic antivirals NA Yes, started preoperatively Antiviral freq if used NA Acyclovir 400 mg 5 times daily or valacyclovir 1000 mg TID for 3 wks then reduced to BID for acyclovir or daily for valacyclovir Previous surgery/procedures NA 2 PK, 1 AlphaCor prosthesis, 4 CE Concurrent surgery Kpro Triple: Kpro, extracapsular CE, posterior chamber NA IOL Range of preoperative VA CF Median: HM 1 ft (20/200 to HM at 1 ft) Range of postoperative VA 20/25 HZK: Median HM at 1 ft (20/60 to NLP) Graft failures No 3 of 4 (all failed from microbial keratitis) Conclusions and comments Kpro is treatment of choice for patients with HZK in Kpro has excellent prognosis in HSV, but not HZK need of corneal transplant

CE, cataract extraction; HSV, herpes simplex keratitis; HZO, herpes zoster ophthalmicus; IOL, intraocular lens; HM, hand motions; NA, not reported; NLP, no light perception; VA, visual acuity.

Copyright Ó 2017 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. Cornea Volume 36, Number 8, August 2017 Management of Corneal Scarring Secondary to HZK scarring due to HZK. The results are summarized in Table 2. Scleral contact lenses may be a useful and perhaps Todani and Gupta reported the case of a 74-year-old woman underused tool in the setting of corneal scarring and severe with corneal scarring due to HZK who was treated with neurotrophic keratopathy. Surgical management in patients Boston keratoprosthesis type 1 combined with extracapsular with a history of HZK achieved good results in some series, cataract extraction and posterior chamber intraocular lens although this seems to rely on appropriate patient selection. placement. Her BCVA improved from counting fingers to Anterior corneal scarring has been treated successfully with 20/25 after 1 month, which was maintained over a 7-month PTK combined with PRK and anterior lamellar keratoplasty. follow-up period.20 Given the requirement for epithelial healing, we believe that Brown et al retrospectively reviewed 4 cases of HZK PTK/PRK should be considered only in the setting of treated with Boston keratoprosthesis type 1. Ages ranged a healthy ocular surface and normal corneal sensation. The from 50 to 65 years. Two eyes had previously failed PKP, and reported cases of anterior lamellar keratoplasty had clear 1 eye had a failed AlphaCor keratoprosthesis. Oral antivirals corneas at last follow-up and did not develop graft rejection were given at the time of surgery followed by long-term use episodes.6,7 This option may be viable for those without at a lower prophylactic dose. All eyes had a glaucoma shunt a history of herpes zoster endotheliitis or scars that preclude placed at the time of surgery, and 3 eyes had revision of their endothelial assessment.29 lateral tarsorrhaphy. Only 1 eye had keratoprosthesis retention Six case series described PKP for visual rehabilitation after a follow-up period of 50.5 months with improvement in secondary to corneal scarring. A majority of these had clear BCVA from hand motions to 20/60. The other 3 eyes grafts at last follow-up. Complications included primary graft developed microbial keratitis and underwent keratoprosthesis failure, graft rejection, exposure keratopathy, bacterial keratitis, explantation after 1, 6, and 15 months. By comparison, this and active inflammation. The reported cases of keratoprosthesis series also reviewed 5 cases of herpes simplex keratitis treated for HZK demonstrated poorer outcomes overall, when com- with a keratoprosthesis that demonstrated a 100 percent pared with the keratoprosthesis for HSV keratitis, with retention rate.21 explantation required in 3 of 4 cases.21 This may be due in part to the secondary effects of severe neurotrophic keratopathy and dry eye syndrome on the ocular surface milieu. Recurrence of Zoster and Effect of Zoster Some studies reported that a longer quiescent period Vaccination before keratoplasty improved the likelihood of graft success. Yawn et al followed a large group of patients with Kosker et al reported a mean quiescent period of 85 months herpes zoster (including any dermatomal involvement) and and reported no graft failures. The mean quiescent period was reported the rate of recurrence at 8 years to be 6.2%.22 Tran shorter in eyes with graft rejection episodes (46 months) et al found the 5-year recurrence rate of herpes zoster compared with eyes without graft rejection (106 months).14 ophthalmicus (including ocular involvement or rash) to be Similarly, Soong et al noted that the 2 cases of graft failure 25%.23 Live-attenuated vaccine administration for zoster is secondary to rejection had shorter quiescent periods of 4 and effective in reducing its incidence by 51.3% according to 11 months, compared with 23 to 112 months for clear grafts.16 a large study.24 Tseng et al showed that vaccination of Lateral suture tarsorrhaphies were placed concurrently immunocompetent patients who have had an episode of with PKP in several cases.14,15,17,18 Reasons given for placing zoster in the past is also beneficial in reducing subsequent suture tarsorrhaphy included a history of persistent corneal episodes.25 The vaccine is similarly effective in reducing epithelial defect, neurotrophic keratopathy, and eyelid abnor- rates of recurrent HZK, but there are also case reports malities; these as well as our recommended indications are describing recurrence soon after patients received the listed in Table 3. Permanent tarsorrhaphy was performed vaccine.26,27 These reports suggest that the increase in less commonly. cell-mediated immunity produced by the vaccine can lead The argon laser was used preoperatively in select to an inflammatory response to viral antigens that persist in neovascularized corneas in an attempt to decrease the risk of the cornea.26–28 Patients with a history of HZK who do get subsequent graft failure.30,31 A majority of these grafts were the live-attenuated vaccine should be monitored in the clear at last follow-up. Other options to preoperatively treat weeks after administration.27 corneal neovascularization include fine-needle diathermy,

DISCUSSION TABLE 3. Indications for Concurrent Tarsorrhaphy at the Time We reviewed the literature regarding the management of Keratoplasty for Herpes Zoster Keratitis of corneal scarring due to HZK. We excluded cases Reasons to consider lateral tarsorrhaphy at the time of surgery describing intervention for active keratitis or corneal melt. Severe dry eye syndrome An important ﬁnding of our review is that there is a lack of Severe neurotrophic keratopathy prospective, randomized studies to provide evidence-based management guidelines. We did ﬁnd that various treatment History of persistent epithelial defect Eyelid abnormalities/exposure keratopathy options for these patients have been described, which are Previous graft failure summarized in this study. The evidence for their use remains somewhat limited at present and requires validation with History of corneal melt/perforation future studies. History of infectious keratitis (excluding HZK)

Copyright Ó 2017 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. Hassan et al Cornea Volume 36, Number 8, August 2017 cryotherapy, and anti-vascular endothelial growth factor agents 3. Yanai R, Nishida T, Chikama T, et al. Potential new modes of treatment (eg, bevacizumab), although to our knowledge, their use has of neurotrophic keratopathy. Cornea. 2015;34:S121–S127. 4. Ladage P, Yamamoto K, Ren D, et al. Effects of rigid and soft contact not been described in the setting of HZK. It should be noted lens daily wear on corneal epithelium, tear lactate dehydrogenase, and that anti-vascular endothelial growth factor agents must be bacterial binding to exfoliated epithelial cells. Ophthalmology. 2001;108: used with caution in the setting of neurotrophic keratopathy.32 1279–1288. Tanure et al reported that 10 of 15 eyes had moderate- 5. Wens M, Koppen C, Tassignon MJ. Scleral contact lenses as an to-severe corneal neovascularization. Of these eyes, 2 devel- alternative to tarsorrhaphy for the long-term management of combined exposure and neurotrophic keratopathy. Cornea. 2013;32:359– oped an endothelial rejection episode, both of which 361. responded well to topical steroids and had clear grafts at last 6. Schornack MM, Pyle J, Patel SV. Scleral lenses in the management of follow-up.17 Although larger studies not specific to HZK have ocular surface disease. Ophthalmology. 2014;121:1398–1405. shown otherwise, Soong et al found that corneal neovascula- 7. Grey F, Carley F, Biswas S, et al. Scleral contact lens management of bilateral exposure and neurotrophic keratopathy. Cont Lens Anterior Eye. rization did not correlate with postoperative graft rejec- 2012;35:288–291. 16,31,33 tion. In that series of 9 patients, 6 had corneal 8. Gumus K, Gire A, Pflugfelder SC. The successful use of Boston neovascularization; 2 patients developed graft rejection, 1 ocular surface prosthesis in the treatment of persistent corneal with superficial vessels peripherally whereas the other had no epithelial defect after herpes zoster ophthalmicus. Cornea. 2010;29: – neovascularization.16 1465 1468. 9. Romero-Rangel T, Stavrou P, Cotter J. Gas-permeable scleral contact Perioperative management in patients with HZK also lens therapy in ocular surface disease. Am J Ophthalmol. 2000;130: included treatments such as artificial tears, punctal plugs, 23–32. topical cyclosporine, and topical steroids. Interestingly, most 10. Rosenthal P, Croteau A. Fluid-ventilated, gas-permeable scleral contact authors either did not mention or did not use oral antivirals in lens is an effective option for managing severe ocular surface disease and many corneal disorders that would otherwise require penetrating the perioperative period. As indicated by the variability in the keratoplasty. Eye Contact Lens. 2005;31:130–134. reported use of these and other agents among published case 11. Dworkin RH, Johnson RW, Breuer J, et al. Recommendations for the series, currently there is no consensus regarding perioperative management of herpes zoster. Clin Infect Dis. 2007;44:S1–S26. medical management. 12. Hamrah P, Cruzat A, Dastjerdi MH, et al. Unilateral herpes zoster A careful discussion of the risks and benefits of zoster ophthalmicus results in bilateral corneal nerve alteration: an in vivo confocal microscopy study. Ophthalmology. 2013;120:40–47. vaccination is required for patients with a history of HZK 13. Kaufman SC. Use of photorefractive keratectomy in a patient with (with and without corneal scarring). Recurrence of herpes a corneal scar secondary to herpes zoster ophthalmicus. Ophthalmology. zoster remains a concern, particularly in those with a history 2008;115:S33–S34. of ophthalmic involvement; although vaccination decreases 14. Kosker M, Duman F, Suri K, et al. Long-term results of keratoplasty in patients with herpes zoster ophthalmicus. Cornea. 2013;32:982–986. the recurrence rate, an increase in cell-mediated immunity 15. Marsh RJ, Cooper M. Ocular surgery in ophthalmic zoster. Eye (Lond). may lead to corneal inflammation in response to persistent 1989;3:313–317. viral antigens. A quiescent period (eg, at least 1 year) should 16. Soong HK, Schwartz AE, Meyer RF, et al. Penetrating keratoplasty for be strongly considered before vaccine administration in the corneal scarring due to herpes zoster ophthalmicus. Br J Ophthalmol. – setting of previous HZK. Close follow-up of recently 1989;73:19 21. 17. Tanure MA, Cohen EJ, Grewal S, et al. Penetrating keratoplasty for vaccinated patients is recommended. varicella-zoster virus keratopathy. 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