Endoscopic Optic Nerve Decompression for Optic Neuropathy in Sinonasal Fibro-Osseous Tumors

Journal Pre-proof Endoscopic optic nerve decompression for optic neuropathy in sinonasal fibroosseous tumors Gwanghui Ryu, Ahmad Zaker Al-Magribi, Kyung Eun Lee, Jung Joo Lee, Sang Bin Kim, Hyo Yeol Kim, Hun-Jong Dhong, Seung-Kyu Chung, Doo-Sik Kong, Sang Duk Hong PII:

S1878-8750(20)30355-7

DOI:

https://doi.org/10.1016/j.wneu.2020.02.080

Reference:

WNEU 14355

To appear in:

World Neurosurgery

Received Date: 17 December 2019 Revised Date:

13 February 2020

Accepted Date: 14 February 2020

Please cite this article as: Ryu G, Al-Magribi AZ, Lee KE, Lee JJ, Kim SB, Kim HY, Dhong H-J, Chung S-K, Kong D-S, Hong SD, Endoscopic optic nerve decompression for optic neuropathy in sinonasal fibro-osseous tumors, World Neurosurgery (2020), doi: https://doi.org/10.1016/j.wneu.2020.02.080. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. 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. © 2020 Elsevier Inc. All rights reserved.

Endoscopic optic nerve decompression for optic neuropathy in sinonasal fibro-osseous tumors

Authors: Gwanghui Ryu1*, Ahmad Zaker Al-Magribi2,3*, Kyung Eun Lee2, Jung Joo Lee2, Sang Bin Kim1, Hyo Yeol Kim2, Hun-Jong Dhong4, Seung-Kyu Chung2, Doo-Sik Kong5, and Sang Duk Hong2

Affiliation: 1

Department of Otorhinolaryngology-Head and Neck Surgery, Soonchunhyang University

College of Medicine, Cheonan, Chungcheongnam-do, South Korea 2

Department of Otorhinolaryngology-Head and Neck Surgery, Samsung Medical Center,

Sungkyunkwan University School of Medicine, Seoul, South Korea 3

Department of Otorhinolaryngology-Head and Neck Surgery, Najran University College of

Medicine, Najran, Saudi Arabia 4

Department of Rhinology, Hana ENT Hospital, Seoul, South Korea

5

Department of Neurosurgery, Samsung Medical Center, Sungkyunkwan University School

of Medicine, Seoul, South Korea

RUNNING TITLE: Endoscopic optic nerve decompression in fibro-osseous tumors

*

Gwanghui Ryu and Ahmad Zaker Al-Magribi contributed equally to this work.

Address for Correspondence:

Sang Duk Hong, MD, PhD. Department of Otorhinolaryngology-Head and Neck Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, South Korea. Address: 81 Irwon-ro, Gangnam-gu, Seoul, 06351, South Korea. Tel: 82-2-3410-3577, Fax: 82-2-3410-6987. E-mail: [email protected]

Funding sources This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (NRF-2017R1D1A1B03031372 to Sang Duk Hong and NRF-2017R1A2B4006453 to Hyo Yeol Kim). This work was supported by the Soonchunhyang University Research Fund.

Conflict of Interest The authors have no conflicts of interest to disclose.

Word count: 2,121

ORCID Gwanghui Ryu: https://orcid.org/0000-0002-3251-399X Kyung Eun Lee: https://orcid.org/0000-0001-8248-2020 Jung Joo Lee: https://orcid.org/ 0000-0002-8078-345X Hyo Yeol Kim: https://orcid.org/0000-0002-2162-3202 Hun-Jong Dhong: https://orcid.org/0000-0003-0054-9629

Seung-Kyu Chung: https://orcid.org/0000-0001-6187-0980 Doo-Sik Kong: https://orcid.org/0000-0002-7519-3594 Sang Duk Hong: https://orcid.org/0000-0003-3075-1035

1

Abstract

2

Backgrounds: Sinonasal fibro-osseous tumors involving the skull base sometimes result in

3

the encasement of the optic canal and can cause the compressive optic neuropathy. The

4

present study aimed to elucidate the optimal timing of endoscopic optic nerve decompression

5

(OND) in cases with optic neuropathy caused by fibro-osseous tumors.

6

Methods: Medical records were reviewed retrospectively from July 2008 and November

7

2016. Subjects who underwent surgery with endoscopic OND for optic neuropathy caused by

8

fibro-osseous lesions were enrolled. Pre- and postoperative ophthalmologic evaluation were

9

analyzed, including best-corrected visual acuity, visual field testing, and color vision.

10

Results: A total of nine patients underwent OND. Seven patients were fibrous dysplasia and

11

two patients were juvenile ossifying fibroma. Patients were male in six cases and female in

12

three cases. The average age was 15 years with a range of 8 to 17 years. Symptom duration

13

ranged from 2 months to 4 years. The mean follow-up period was 28 months (range, 0.8 to

14

76.4 months). There was no immediate deteriorated vision after OND. Eight eyes (88.9%)

15

were improved and one eye (11.1%) had only visual field improvement. However, patients

16

whose visual impairment was in the range of finger count and hand motion were not

17

recovered beyond the quantitatively measurable level even after OND.

18

Conclusion: Endoscopic OND in patients with optic neuropathy caused by a fibro-osseous

19

tumor in the sinonasal region is safe and worth trying to improve visual outcomes. Early

20

therapeutic OND is recommended before the patient’s visual function is decreased below

21

quantitatively measurable vision.

22 23

Key words: Fibro-osseous tumor, sinonasal, optic neuropathy, optic nerve decompression,

24

endoscopic surgery

25 1

26

2

27

Introduction

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Fibro-osseous tumors in the sinonasal area can encase the optic canals because the lesions

29

frequently affect the skull base in the craniofacial region.1 Loss of vision caused by optic

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nerve compression is the most devastating symptom and significantly reduces the quality of

31

life in patients with sinonasal fibro-osseous tumors.2 The two most common histopathologies

32

are fibrous dysplasia (FD) and ossifying fibroma (OF), which can involve optic canal in the

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sinonasal region. The other subtypes are osteoma, bone cysts, and osteosarcoma.3, 4 Many

34

studies investigated optic neuropathy in patients with FD.5 Despite optic nerve constriction,

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95% of FD patients have no visual symptoms and signs and most patients are asymptomatic

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during follow-up periods.6 Therefore, it is established knowledge that prophylactic optic

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nerve decompression (OND) is not recommended for sinonasal fibro-osseous lesions.7, 8

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OND is a major treatment option for symptomatic optic neuropathy caused by optic nerve

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compression secondary to fibro-osseous tumors.9 Recent advances in endoscopic surgery and

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image-guided navigation systems have enabled more meticulous OND surgery since

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Luxenberger et al. reported their experiences with endoscopic endonasal approaches for

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traumatic OND in 1998.10 Nevertheless, vision preservation in the management of fibro-

43

osseous lesions that compress the optic nerve is still challenging. The risks of surgical

44

treatment include worsening of vision or blindness that should be considered when surgeons

45

are deciding on OND surgery. However, there has been no consensus regarding the optimal

46

timing for OND surgery, and it is usually determined by the surgeon on a case by case basis.

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The present study aimed to review the surgical outcomes of endoscopic OND in a case series

48

of sinonasal fibro-osseous tumors and to suggest the optimal timing and surgical indications

49

for endoscopic OND based on pre-operative ophthalmologic evaluation of patients’ visual

50

function. 3

51 52

Materials and methods

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Study Subjects

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Medical records were reviewed retrospectively from July 2008 and November 2016. Subjects

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who were diagnosed with fibro-osseous tumors in the sinonasal regions that were surrounding

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the optic nerve and who had optic neuropathy confirmed by ophthalmologists were enrolled.

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A malignant case such as osteosarcoma was excluded. Among them, patients who underwent

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therapeutic endoscopic OND that included the results of pre- and postoperative

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ophthalmologic evaluation were analyzed. All patients were evaluated according to best-

60

corrected visual acuity (BCVA) and severe visual loss was defined as BCVA ≤ 20/200.11

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Visual acuity levels below the quantitative measurements were defined using the

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semiquantitative ordinal scales of finger count and hand motion.12 Visual fields were

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evaluated using a Humphrey Visual Field Analyzer (Humphrey Instruments, San Leandro,

64

CA, USA). Visual fields were measured as the mean deviation difference between patient

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scores and the normal values expected for the patient’s age group. The normal range is 0 dB

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to -2 dB and severe defects are scored under -11 dB.13 Color vision was tested with 15

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Ishihara color plates. This study protocol was approved by the Institutional Review Board of

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Samsung Medical Center (IRB No. SMC 2019-01-107) and informed consent was waived.

69 70

Endoscopic Optic Nerve Decompression

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The majority of endoscopic ONDs were performed by both a rhinology surgeon and

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neurosurgeon. An image-guided navigation system was used in all cases. The detailed

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surgical procedures varied case by case. Complete ethmoidectomy was performed to identify

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the disease occupying lesion in the posterior ethmoid sinus or sphenoid sinus. First, fibro4

75

osseous tumors were removed as much as possible in the sinonasal cavity to expose the skull

76

base and optic canal using cold instruments or powered instruments, including drills and

77

microdebriders. After controlling bleeding from the tumor, the fibro-osseous lesion of the

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anterior portion of the optic nerve was removed with a high-speed drill using a 3 mm

79

diamond burr. Tumorous lesions around bony canal were paper-thinned and removed by

80

Kerrison punch or curette from the midline dura to orbital apex (Figure 1). The goal was to

81

remove bony lesion around the encased optic nerve as much as possible without causing

82

nerve sheath injury. In some cases, the sphenoid bone or anterior clinoid process was well

83

pneumatized, allowing removal of 360 degrees of the bony lesion. The optic nerve sheath was

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left un-incised and all cases underwent extradural decompression of the optic canal.

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Nonabsorbable packing materials were used (Nasopore®; Polyganics BV, Groningen,

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Netherlands). Preoperative computed tomography images were presented in Figure 2.

87 88

Statistical Analysis

89

Statistical analyses used in this study include the Wilcoxon matched-pairs signed-rank test. A

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P value of less than .05 was considered statistically significant for all analyses. Analyses were

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performed using Stata software v14.0 (StataCorp LP, College Station, TX).

92 93

Results

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Nine patients with 9 eyes who underwent endoscopic OND were analyzed. Patients were

95

male in 6 cases and female in 3 cases. The average age was 15 years with a range of 8 to 17

96

years. Seven patients were FD and 2 patients were juvenile OF. No patient was diagnosed

97

with McCune-Albright syndrome. One OF patient was initially diagnosed as OF who

98

developed malignant transformation (osteosarcoma) with compressive optic neuropathy. The 5

99

mean follow-up period was 28 months (range, 0.8 to 76.4 months).

100

Demographic data and ophthalmologic evaluation results are described in Table 1. Visual

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symptom duration between onset and surgery ranged from 2 months to 4 years and they had a

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progressive aggravation of visual loss. All symptomatic patients had decreased visual acuity

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and only 4 eyes were above quantitatively measurable vision and they had a relatively shorter

104

duration (5.5 ± 4.7 months) than the others (17.8 ± 7.6 months) without statistical

105

significance (p = 0.102). The BCVA of five eyes was less than finger count and they also had

106

severe visual field defects. The color vision test was not performed in all cases and only 5

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patients had pre-and postoperative results. There was a slight improvement in color vision in

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2 patients.

109

When comparing visual outcomes between before and after OND, there was no immediate

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deterioration of vision, while 8 eyes (88.9%) were improved and one eye (11.1%) had only

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visual field improvement. Patients whose visual impairment was in the range of finger count

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and hand motion were not recovered beyond the quantitative measurable level after OND,

113

although the optic nerve was fully decompressed (Figure 3). Pre- and postoperative BCVAs

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and visual field mean deviations were significantly improved (p = 0.031 and p = 0.031,

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respectively) after OND surgery (Figure 4). Three FD patients (Case No. 2, 4, and 5) had

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tumor regrowth and 1 patient (Case No. 2) underwent revision tumor removal surgery. No

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patients experienced major complications after OND surgery such as severe bleeding,

118

infection, cerebrospinal fluid leakage, or cranial nerve palsy.

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Several articles have reported visual outcomes of endoscopic OND in patients with sinonasal

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fibro-osseous tumors and we summarized the results in Table 2.9, 14, 15 We identified 11 cases

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and 13 eyes. Only 4 eyes (30.8%) had a severe visual loss (BCVA ≤ 20/200), whereas the

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visual acuity of 6 out of 9 cases (66.7%) revealed severe visual loss in this study. Data of time

123

to intervention was available in 7 out of 13 eyes, and it was relatively shorter (8 to 75 days) 6

124

compared with subjects in this study (2 months to 1 year). All cases had good surgical

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outcomes in postoperative evaluation.

126 127

Discussion

128

In this retrospective review of nine sinonasal fibro-osseous tumor patients, all cases

129

underwent endoscopic OND without any significant complication or surgery-related visual

130

deterioration. A sinonasal fibro-osseous tumor is a rare disease and surgical cases that require

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tumor removal with OND are extremely rare. It is very difficult for surgeons to determine the

132

optimal timing and extent of surgery. Although OND is not indicated for prophylactic

133

purposes in the case of optic nerve encasement,6 it is not clear when OND should be

134

performed if a visual function is decreased. Encasement of the optic nerve does not progress

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with age in general and increasing age does not necessarily bring the likelihood of optic

136

neuropathy and blindness.16 Therefore, radiologic evidence of optic nerve encasement with

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fibro-osseous tumors does not provide clues as to whether the visual loss will develop. In a

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large retrospective cohort study, only 12% of patients with complete optic nerve involvement

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had optic neuropathy.16 Although symptomatic optic neuropathy is infrequent, fibro-osseous

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tumor patients with optic nerve encasement need regular follow-up and routine

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ophthalmologic evaluation.

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In this case series, the majority of patients had severe visual loss and only four patients

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underwent OND surgery before visual acuity was decreased below quantitatively measurable

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vision. Several possible reasons were that the patient did not notice visual loss because the

145

symptoms developed slowly and unilaterally, and they did not visit the hospital regularly. In

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addition, the surgeon hesitated to perform the surgery because of potential complications such

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as aggravation of visual loss or blindness in the early period.8, 17 Patients in the present study, 7

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whose visual acuity in the range of finger count and hand motion preoperatively were not

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recovered beyond quantitatively measurable vision even after OND. Patients who had fewer

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visual deficits showed favorable results including visual acuity and visual field tests. In the

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literature review, most cases had shorter symptom duration and less visual impairment

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compared to subjects in this study (Table 2). At last, favorable visual outcomes were obtained

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even in patients with severe visual loss. While we cannot directly compare the relationship of

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symptom duration and visual outcome between our patients and subjects in the previous

155

papers, short symptom duration seems to affect postoperative prognosis. If patients become

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symptomatic or have obvious optic neuropathy, early surgical intervention is mandatory to

157

restore vision.

158

Before endoscopic OND surgery, a precise understanding of the aberrant anatomy in each

159

case is important. The endonasal trans-sphenoethmoidal approach can provide excellent

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visualization from the orbital apex to the optic chiasm. Although FD cases do not require

161

complete removal of tumorous tissues, it is recommended to decompress the optic nerve

162

around all 360 degrees.18 In this case series, 3 FD patients experienced tumor regrowth during

163

the follow-up period. After nearly total decompression of the optic canal, the risk of optic

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nerve compression can be reduced even if the tumor grows. Juvenile OF need gross total

165

removal of tumors to prevent a recurrence. Juvenile OF is usually rapidly growing, locally

166

destructive, and easily recurs.19 One OF patient from this study had tumor recurrence with

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compressive optic neuropathy after the initial surgery, and the final pathologic diagnosis was

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osteosarcoma. Even if the tumors are completely removed, regular follow-up is necessary for

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juvenile OF patients.20

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Favorable surgical outcomes for therapeutic decompression have been reported in several

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case series. Tan et al. reviewed 11 FD cases; five nerves were improved and deterioration was

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prevented in six nerves after therapeutic OND (surgical methods were not indicated).21 A case 8

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report of therapeutic OND in an FD patient who had only visual field defects without other

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abnormalities had a complete recovery after surgery.22 Another case series reported that all 4

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nerves improved and all patients had normal visual acuity after therapeutic endoscopic OND

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(Table 2).9 Preoperatively, 3 cases had mild visual loss and 1 case had a profound visual loss

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(visual acuity: 20/500) as defined in this paper. In contrast, none of the patients in this case

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series had visual loss less than finger count whereas more than half of patients in this study

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had decreased visual acuity less than finger count. Some authors recommend that OND

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surgery should be undertaken early in the disease course before optic nerve atrophy.15 These

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findings suggest that early therapeutic OND in patients with mild visual deficits can achieve

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good ophthalmologic outcomes. Additionally, there may be a certain role of OND in patients

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with visual acuity in the range of finger count, hand motion, or light perception. A sudden

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worsening of vision can be recovered after OND surgery even if blind, and some degree of

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recovery may improve the patient’s quality of life.

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The present study described the benefit of endoscopic OND with a case series of sinonasal

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fibro-osseous tumors from one tertiary referral hospital. However, there are some limitations.

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First, a complete ophthalmologic evaluation before and after surgery was not performed in all

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cases. Second, additional ophthalmologic examination such as optical coherence tomography

190

(OCT) may be helpful in determining surgery and predicting surgical outcomes. Abnormal

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results on OCT is associated with the presence of optic neuropathy.23 OCT can provide a

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prognosis of visual outcome studied with compressive optic neuropathy caused by pituitary

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adenomas.24, 25 Furthermore, a limited number of patients and a heterogeneous disease group

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make interpreting the results complicated.

195 196

Conclusion 9

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Endoscopic OND in patients with optic neuropathy caused by a fibro-osseous tumor in the

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sinonasal region is relatively safe and worth trying to achieve good visual outcomes. Patients

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who have complete optic nerve encasement need regular follow-up and ophthalmologic

200

evaluation. If compressive optic neuropathy caused by fibro-osseous tumors is confirmed,

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OND should be performed as soon as possible to achieve a better visual outcome.

202 203

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Figure Legends

293 294

Figure 1. (A) Preoperative CT scan of a representative patient (Case No. 4). The patient had

295

compressive optic neuropathy of the left optic nerve (white arrow). (B) Endoscopic view of

296

left optic nerve decompression. (C) Postoperative CT of decompressed optic nerve (white

297

arrow).

298

ACP = anterior clinoid process; ON = optic nerve

299 300

Figure 2. Preoperative CT images for Case No. 1, 2, 3, 6, 7, and 8. White arrow indicates

301

compressed optic nerve by the lesion.

302 303

Figure 3. (A) Pre- and postoperative CT scan of Case No. 5. (B) Visual acuity and visual

304

field were improved but visual acuity could not be improved beyond quantitatively

305

measurable vision. (C) Pre- and postoperative CT scan of Case No. 9. (D) Visual acuity and

306

visual field were improved after surgery.

307 308

Figure 4. (A) Pre- and post-operative visual acuity. (B) Pre- and post-operative visual field.

309

VA = visual acuity; Fc = finger count; Hm = hand motion

310

15

Table 1. Pre- and postoperative ophthalmologic evaluation Preoperative evaluation Diagnosis Age Sex Eye Visual field Color BCVA (dB) vision 1 FD 16 Male OS 1 year 20/32 normal n/c 2 FD 8 Female OD 6 months 20/125 -5.19 15/15 3 FD 13 Male OD 2 months 20/125 -20.64 0/15 4 FD 15 Male OS 2 months 20/250 -16.88 13/15 5 FD 15 Male OS 4 years Fc/10 cm -31.31 0/15 6 FD 16 Female OD 1 year Fc/10 cm -33.86 0/15 7 FD 16 Male OD 11 months Hm n/c 0/15 8 OF 17 Female OD 6 months Hm -34.39 n/c 9 OF 17 Male OS 1 year Fc/30 cm -34.47 0/15 * Duration between symptom onset and optic nerve decompression surgery. Case No.

Visual loss duration*

Postoperative evaluation Visual field Color BCVA (dB) vision 20/25 normal n/c 20/100 -4.27 15/15 20/125 -14.14 1/15 20/40 -3.47 15/15 Fc/50cm -23.69 0/15 Fc/30 cm n/c 0/15 Fc/20 cm n/c n/c 20/630 -18.76 n/c 20/630 -29.39 n/c

BCVA, best-corrected visual acuity; Fc, finger count; FD, fibrous dysplasia; Hm, hand motion; n/c= not checked; OD, right eye; OF, ossifying fibroma; OS, left eye

Table 2. Pre- and postoperative visual acuity in patients with sinonasal fibro-osseus tumors from literature review Case No. 1 2 3 4

Author DeKlotz et al.9 DeKlotz et al. DeKlotz et al. DeKlotz et al.

Age

Diagnosis

47 18 16 21

FD FD FD FD

Eye

OS OS OS OD OS 5 Liu et al.14* 10 MAS OS 6 Liu et al. 17 FD OS OD 7 Liu et al. 55 FD OD 8 Liu et al. 21 FD OS 9 Liu et al. 19 OF OS 10 Liu et al. 29 OF OS 11 Berhouma et al.15* 27 OF n/a * Decimal data were converted into 20 feet fraction scale. †

Visual loss duration† 75 days 60 days 14 days 8 days 8 days n/a 25 days 25 days n/a n/a n/a n/a n/a

Visual acuity Preoperative Postoperative 20/50 20/20 20/20 20/15 20/500 20/20 20/25 20/20 20/25 20/20 20/160 20/32 Lp 20/30 No Lp 20/63 20/25 20/16 20/32 20/20 20/200 20/32 20/50 20/25 20/32 20/25

Duration between symptom onset and optic nerve decompression surgery.

FD, fibrous dysplasia; Hm, hand motion; n/a= not available; MAS, Lp, light perception; McCune-Albright syndrome; OD, right eye; OF, ossifying fibroma; OS, left eye

Abbreviations BCVA: Best-corrected visual acuity FD: Fibrous dysplasia OF: Ossifying fibroma OND: Optic nerve decompression

Declaration of interests ☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. ☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

Credit Author Statement Conceptualization: GR, AZA, SDH, Data curation: KEL, JJL, Formal analysis: GR, AZA, Funding acquisition: GR, HYK, SDH, Methodology: HYK, HJD, SKC, Visualization: GR, DSK Writing – original draft: GR, AZA, SDH, Writing – review & editing: HYK, HJD, SKC, DSK, SDH