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Spontaneous Blinking Kinetics on Paralytic Lagophthalmos After Lid Load with Gold Weight or Autogenous Temporalis Fascia Sling a
ab
ab
Sarah P. F. Wambier , Denny M. Garcia , Antonio A. V. Cruz
a
& Andre Messias
a
Department of Ophthalmology, Otorhinolaryngology, Head and Neck Surgery, Ribeirão Preto Medical School, University of São Paulo, Sao Paulo, Brazil and b
Craniofacial Research Support Center, University of São Paulo, Sao Paulo, Brazil Published online: 27 May 2015.
Click for updates To cite this article: Sarah P. F. Wambier, Denny M. Garcia, Antonio A. V. Cruz & Andre Messias (2015): Spontaneous Blinking Kinetics on Paralytic Lagophthalmos After Lid Load with Gold Weight or Autogenous Temporalis Fascia Sling, Current Eye Research To link to this article: http://dx.doi.org/10.3109/02713683.2015.1031252
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Current Eye Research, Early Online, 1–8, 2015 ! Informa Healthcare USA, Inc. ISSN: 0271-3683 print / 1460-2202 online DOI: 10.3109/02713683.2015.1031252
ORIGINAL ARTICLE
Spontaneous Blinking Kinetics on Paralytic Lagophthalmos After Lid Load with Gold Weight or Autogenous Temporalis Fascia Sling Sarah P. F. Wambier1, Denny M. Garcia1,2, Antonio A. V. Cruz1,2 and Andre Messias1
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1
Department of Ophthalmology, Otorhinolaryngology, Head and Neck Surgery, Ribeira˜o Preto Medical School, University of Sa˜o Paulo, Sao Paulo, Brazil and 2Craniofacial Research Support Center, University of Sa˜o Paulo, Sao Paulo, Brazil
ABSTRACT Purpose: To assess the upper eyelid kinematics during spontaneous blinking in unilateral paralytic lagophthalmos before and after upper eyelid load with gold weight (GW) or autogenous temporalis fascia (TF) sling. Design: Comparative case series. Subjects: Patients with long-standing unresolved unilateral facial palsy who underwent surgical treatment with GW (n = 8) or upper lid cerclage with TF (n = 10). The contralateral eyelid served as the control for each patient (control group). Methods: Preoperative and postoperative measurements of spontaneous blink kinematics with magnetic search coil and clinical assessment of lid margin position, lagophthalmos and ocular surface exposure, and determine amplitude, maximum velocity and main sequence of spontaneous blinks; relative amplitude of blinks to the pupil center; ocular surface exposure scores; magnitude of lagophthalmos and mid-pupil lid distances. Results: The mean (±SE) down-phase amplitude ratio between paralyzed and contralateral eyelids (blink gain) was 10.0% preoperatively for both groups and significantly increased to 29 ± 6% for the GW group (p50.05) and 23 ± 4% for the TF group (p50.05). At 6 months the gain was significant for the GW group only (32 ± 7%, p50.05). There was no effect on the maximum velocity of the blinks or the main sequence of paretic and contralateral blinks with either surgery. Both procedures lowered the lid margin increasing the number of blinks that reached the pupil center. At 6 months this effect was prominent only for the GW group. Exposure keratopathy scores and lagophthalmos decreased postoperatively especially in the GW group. Conclusions: The beneficial effect of lid load surgeries result from a combination of a small increase on the spontaneous blink amplitude and a static effect due to the reduction of the distance between the lid margin and pupil center. Keywords: Facial palsy, gold weight, lid loading, paralytic lagophthalmos, spontaneous blink, upper eyelid kinematics, upper eyelid sling
INTRODUCTION
believed that hares and rabbits (lagomorph animals) slept with open eyes,1 this term is a pictorial description of the upper lid retraction and poor lid kinetics that accompanies defective upper lid closure.
The word ‘‘lagophthalmos’’ originates from the Greek and literally means hare’s eye.1 As the ancient Greeks
Received 15 September 2014; revised 28 January 2015; accepted 12 March 2015; published online 25 May 2015 Correspondence: Andre Messias, Department of Ophthalmology, Otorhinolaryngology, and Head and Neck Surgery, Ribeira˜o Preto Medical School, University of Sa˜o Paulo, Av. Bandeirantes, 3900, 14049-900 Ribeira˜o Preto, SP, Brazil. Tel: +55 1636022865. Fax: +55 1636022860. E-mail: [email protected]
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Paralytic lagophthalmos occurs when the orbicularis oculi muscle is denervated. In this condition, spontaneous blinks are severely affected and may be virtually absent in cases of complete paresis. The longterm effects of a defective spontaneous blinking activity are devastating for the ocular surface. Exposure keratitis, corneal ulcers and eventually blindness are potential ophthalmic consequences of peripheral facial palsy.2 Restoration of eyelid kinetics in the setting of orbicularis palsy is a difficult problem, which has been addressed by various surgical and non-surgical procedures including the use of magnets,3 springs,4–6 electrical stimulation,7 temporalis muscle transfer,8 eyelid cerclage with silicone bands9 and lid-loading operations.10–12 Although the literature on the different treatment modalities is vast, we are aware of only one study that employed magnetic search coil to quantify the effect of gold weight (GW) implants on spontaneous blink kinetics in six patients.13 In this study, we compared the spontaneous blink metrics after lid loading with GW and upper lid sling with temporalis fascia (TF) on a sample of patients with unresolved facial palsy.
METHODS The study protocol adhered to the tenets of the Declaration of Helsinki and was approved by the local Institutional Review Board. All participants gave written informed consent before entering into the study.
Patients and Groups Eighteen consecutive patients with unilateral irreversible longstanding (mean time = 8 years) facial palsy were enrolled in the study. All patients had grade IV to V facial nerve dysfunction on the House and Brackmman scale with incomplete eye closure and symptoms of eye exposure. The etiologies of the facial palsy were excision of acoustic neuroma or extracranial tumors (n = 13), head trauma (n = 2), congenital (n = 2) and idiopathic (n = 1). Two patients had decreased lacrimal secretion (Schirmer test 55 mm) and one patient had corneal anesthesia. All patients underwent an informed consent that explained the risks and benefits of the surgical procedures. The patients were randomly assigned to undergo either standard pretarsal GW lid procedure (GW group, n = 8) or upper lid sling with TF (TF group, n = 10). The contralateral eyelid served as the control (control group). Both groups had the same gender ratio (1:1). The mean age was 49 years (range, 33–70 years) for the
GW group and 45.9 years for the TF group (range, 27–69 years).
Surgeries In the GW group all patients surgery was performed with a standardized pretarsal fixation of gold implants of 1.0 g (n = 5) or 1.2 g (n = 3) measuring approximately 10 mm length, 5 mm height and 2 mm thickness.14 The TF group underwent a modification of the original Arion technique15 as suggested by McCord and Codner.16 A 30-mm length, 5-mm height strip of TF is removed from the patient’s temporal fossa. A lid crease incision is used to raise a pretarsal skin–muscle flap in order to expose the whole tarsal plate from the upper limb of the medial canthal tendon to lateral insertion of the lateral retinaculum on the lateral orbital rim. The medial end of the fascia is first sutured with non-absorbable suture to the upper limb of the medial canthal tendon. Then, the fascia strip is stretched over the tarsal plate and sutured under tension on the periosteum of the lateral orbital rim at the level of the Whitnall’s tubercle17 creating a strong downward vector on the upper eyelid.
Ophthalmological Examination Preoperatively, and on the first and sixth postoperative months, all patients had a comprehensive ophthalmic examination with special attention to the upper eyelid position, exposure keratopathy and degree of lagophthalmos. Lid margin position relative to the pupil center (mid-pupil lid distance or MPLD) was measured on digital images of the palpebral fissure on primary gaze position with the Image J 1.45 software (National Institute of Health, Bethesda, MD, USA). Digital photography was performed with a Nikon D5000 camera (Nikon Inc., Tokyo, Japan) equipped with a macro Nikkor 60 mm lens. A millimeter ruler was included on the images for pixel/mm conversion. Lagophthalmos was defined as any gap between the upper and lower lids following gentle closure of the fissure. The degree of lagophthalmos was measured with the same equipment used to quantify the MPLDs. Exposure keratopathy was quantified by the degree of corneal staining with fluorescein as described by Lemp.18 The cornea was divided in five areas and a standardized 0–3 system was used for each area of the cornea. The sum of the scores was the keratopathy measurement.
Eyelid Kinematics Recording Spontaneous blinks of both eyes of all patients were registered with the magnetic search coil technique as Current Eye Research
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Spontaneous Blinking Kinetics on Paralytic Lagophthalmos described previously.19 Briefly, subjects were seated comfortably with the head stabilized on a chin rest in a weak magnetic field. Small coils (3.8 mm diameter, 30 turns, 30 mg, copper wire 0.102 mm in diameter) were taped to the center of the pretarsal area of the upper eyelids. The recordings were low-pass filtered at 10 kHz, amplified 20,000 times, digitized with 12-bit precision and sampled at 200 Hz with a computer driven system (Remel Laboratories, San Antonio, TX), that resolved spatial changes in lid rotations as small as 0.18 (equivalent to a linear lid motion of 0.02 mm) every 5 ms. Spontaneous blinks of paretic and contralateral lid were recorded continuously for 5 min, while the subjects watched the same video (commercial movie). Specific software (programmed in C# language) was used to analyze the data. An algorithm based on the derivatives of the blink signal detected the blinks automatically. In addition, the data retrieved were checked manually to avoid mistakes. For each blink, the software calculated the amplitude (degrees) and maximum (peak) velocity ( /s) of the closing phase of the movements. Linear regression was used to fit the main blink sequences (relationship between amplitude and maximum velocity).19 The parameters values of the paretic lid movements were expressed as a percentage of the same parameter of the contralateral normal blinks. This ratio (value of the movement of paretic lid/value of movement of the normal lid) was referred to as blink gain.20 In order to express the lid motion relative to pupil center blink amplitudes were also converted to millimeters according to the well-known formula A = r sin (A0 ), where A is amplitude in mm, r is the radius of the globe (assumed to be 12 mm) and A0 is the amplitude in degrees. The converted amplitudes were then divided by the mid-pupil lid distances. We named this variable ‘‘relative amplitude’’ and blinks with relative amplitude = 1 reached the pupil center. Values 51 and 41 indicate movements, which did not attain or covered the pupil center, respectively.
Statistics Two-way analysis of variances (group across time) with post hoc Tukey–Kramer HSD tests was used to compare the effect of surgery on the degree of lagophthalmos and corneal staining, MPLD, blink kinetics (amplitude, maximum velocity and main sequence) at 1 and 6 months postoperatively. Standard error was used to indicate mean variability throughout the text. All statistical procedures were performed using JMP SAS 11.0 (SAS Institute, Inc., Cary, NC). A p value less than 0.05 was considered statistically significant. !
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RESULTS Eye Surface Scores and Lagophthalmos Measurement The corneal exposure scores were 7.6 ± 1.3 and 7.5 ± 1.4 at baseline, and decreased significantly for both groups over time (F = 24.49, p50.001), to 3.4 ± 0.7 and 1.4 ± 0.5 at 1 month postoperatively, and to 2.8 ± 0.6 and 1.5 ± 0.5 at 6 months postoperatively, for GW and TF groups, respectively. Mean lagophthalmos at baseline was 8.9 ± 0.7 and 8.3 ± 0.7 mm, for the GW and TF groups, respectively, and also decreased significantly postoperatively for both groups (F = 90.14, p50.0001). However, the effect was significantly greater on the GW group (7.73, p = 0.009), which decreased 1.2 ± 0.7 and 3.0 ± 0.9 mm, for GW and TF groups, respectively, 1 month after treatment. The interaction group across time was also significant (F = 4.17, p = 0.025), and at 6 months, lagophthalmos was significantly smaller for GW group: 1.4 ± 0.9 mm, while TF = 3.8 ± 0.8 mm (p50.05 TW group and p40.05 TF group).
Eyelid Kinematics Preoperative spontaneous blink parameters are presented in Table 1. The amplitude of the paretic blinks was less than 20% of the contralateral lids in all but one patient (TF #6). These small blinks were also very slow. The mean slope of relationship between amplitude and maximum velocity was 30% and 48% of the control group for the GW and TF groups, respectively. Blink amplitudes of all paretic lids increased 1 month after lid load with GW (Figure 1), and at 6 months this increase was lost in just one patient, (#7) who showed mean blink gain smaller than preoperatively. High gains were observed in two patients (#4 and #5), and in 50% of the eyes, the amplitude was equal to or greater than 30% of the contralateral lid. In the TF group, the long-term increments of the blink amplitudes were more modest. At 6 months postoperatively, the gains of all cases in the TF group were below 30% and similar to the GW group, in one patient (#5) the gain completely regressed. Mean preoperative amplitude gain (0.10 for both groups) increased to 0.29 ± 0.06 and 0.23 ± 0.04, for GW and FT, respectively, at 1 month postoperatively. ANOVA indicated the factor time was significant (F = 14.23, p50.0001) and the post hoc Tukey test confirmed that, at 6 months postoperatively, the mean gain (0.32 ± 0.07) in the GW group was significantly greater than its baseline value (p = 0.0013), but this effect was not significant in the TF group (0.19 ± 0.03) (p = 0.4538). Table 2 presents the mean values of the main sequence slopes for the paretic and contralateral
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TABLE 1 Preoperative spontaneous blinks parameters for all patients. Paretic eyelid
Group Patient
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GW
1 2 3 4 5 6 7 8
Mean ± SE TF 1 2 3 4 5 6 7 8 9 10 Mean ± SE
N 32 56 177 60 28 255 40 82 91.3 ± 28.9 30 204 32 67 63 34 66 17 29 109 65.1 ± 17.7
Contralateral eyelid
Blink gain (ratio paretic/normal)
Main Main Maximum Main Amplitude Maximum sequence Amplitude Maximum sequence Amplitude velocity sequence velocity ( /s) (1/s) ( ) velocity ( /s) (1/s) ( ) ( /s) (1/s) ( ) 1.6 3.7 2.5 3.7 3.2 2.3 3.7 3.6
58.5 58.5 53.7 62.3 59.5 68.7 65.7 45.7
NS 5.2 6.6 4.8 6.8 5.4 6.8 1.4
27.4 45.0 32.4 44.0 17.9 19.3 25.9 48.8
562.5 877.4 663.7 879.2 261.1 572.9 476.8 1223.4
3.0 ± 0.3 5.6 1.5 2.1 1.6 2.7 4.3 1.0 4.5 3.7 1.4 2.8 ± 0.5
59.1 ± 2.5 58.5 41.2 78.8 66.0 36.4 74.4 21.0 82.5 54.8 30.3 54.4 ± 6.8
5.3 ± 0.7 3.2 5.1 NS 10.3 NS 10.0 7.1 14.2 7.5 11.5 8.6 ± 1.1
32.6 ± 4.3 39.5 41.3 28.9 18.0 25.9 16.4 17.0 50.7 28.9 27.0 29.4 ± 3.6
32.6 13.2 28.3 14.1 17.5 30.9 13.2 22.7
0.06 0.08 0.08 0.08 0.18 0.12 0.14 0.07
689.6 ± 104.8 21.6 ± 2.9 0.10 ± 0.01 772.4 22.0 0.14 999.8 22.5 0.04 768.5 28.9 0.07 505.9 24.4 0.09 447.8 NS 0.10 212.7 6.9 0.26 428.0 28.6 0.06 917.7 44.0 0.09 393.3 NS 0.13 689.7 22.5 0.05 613.6 ± 80.2 25.0 ± 3.3 0.10 ± 0.02
0.10 0.07 0.08 0.07 0.23 0.12 0.14 0.04
– 0.39 0.23 0.34 0.39 0.17 0.52 0.06
0.11 ± 0.02 0.30 ± 0.06 0.08 0.15 0.04 0.23 0.10 – 0.13 0.42 0.08 – 0.35 1.45 0.05 0.25 0.09 0.32 0.14 – 0.04 0.51 0.11 ± 0.03 0.48 ± 0.14
NS, Nonlinear relationships (slopes with p40.05).
blinks before and after surgery. Although slopes of paretic blinks on the TF group were significantly higher than in the GW (F = 5.91, p = 0.03), neither the factor time (paretic F = 1.56, p = 0.23, contralateral F = 0.47, p = 0.63) nor the interaction time versus group (paretic F = 0.16, p = 0.86, contralateral F = 1.81, p = 0.18) was significant for both lids. Figure 2 shows an example of the stability of the main sequence of the paretic and normal lid. The relative amplitude of the blinks is dependent on the values of blink amplitude and the static position of the lid. As shown in Table 3, the mean MPLD decreased on the first postoperative month on both groups (p50.001), but at 6 months this MPLD was not significantly different from baseline for the TF group (p = 0.2520). The diminished effect of the FT on MPLD with time coupled with the smaller blink gain induced by the surgery explains the striking difference between the groups regarding the relative amplitude of the blinks. At 6 months postoperatively, 47% of the blinks in the GW group had amplitudes large enough to cover the pupil center while only of 0.7% blinks from the lids in the TF group had the same level of effectiveness. As expected, the mean relative amplitude of the GW group was statistically significantly greater than baseline at 1 month postoperatively (p = 0.0186), and showed statistical significance at 6 months (p = 0.05), but this effect was not observed for the TF group (1 month: p = 0.6777; 6 months: p = 0.9887).
DISCUSSION Spontaneous blinks are highly conjugate bilateral movements. In normal subjects the variability in amplitude between eyes is narrow with gains ranging from 0.8 to 1.2. Acute orbicularis palsy introduces an abrupt asymmetry to blinking. As the innervation to the orbicularis muscle is suppressed, the active force that generates the closing phase of the blinks disappears and the only forces capable of lowering the paretic eyelid margin are those generated by the relaxation of the levator palpebral superioris muscle.21 Our results concur with previous observations that in severe long-standing unresolved orbicularis palsy, the abnormal blinks observed in the affected lids represent passive movements.20 In general, these blinks have small amplitudes (in our sample the mean gain was just 0.1) and low velocity–amplitude relationships. Notably, although the range of amplitude of the paretic blinks was limited, only 16.7% of their main sequences could not be fitted by linear regression lines. In all but one case, the slopes of these main sequences were less than half of the slopes of the contralateral (control) lids. The blink metrics of the unaffected lids were all within the normal range.19 This finding confirms previous suggestions that compensatory hyperactive phenomena, seen in the unaffected lids of patients with mild facial palsy,22 are not recruited when the facial palsy is severe. Current Eye Research
Spontaneous Blinking Kinetics on Paralytic Lagophthalmos
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Gold Weigh 0.7
0.6
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BL 1M 6M BL 1M 6M BL 1M 6M BL 1M 6M BL 1M 6M BL 1M 6M BL 1M 6M BL 1M 6M
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FIGURE 1 Effect of gold weigh (top) and upper eyelid TF cerclage (bottom) on the gain of spontaneous blink amplitude. Baseline preoperative values (BL) and postoperative changes at one (1M) and six months (6M).
TABLE 2 Mean slopes of the main sequence (1/s). Paretic lid BL
1m
Normal lid 6m
BL
1m
6m
GW 5.3 ± 0.7 6.6 ± 1.0 7.2 ± 1.0 21.6 ± 2.9 22.7 ± 2.9 24.3 ± 3.3 TF 8.6 ± 1.1 8.9 ± 1.0 10.0 ± 1.4 25.0 ± 3.3 18.7 ± 3.0 18.6 ± 2.3
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The most common treatment modalities of paralytic lagophthalmos are based on the increment of the passive eyelid forces stored by the elastic components of the lid. With GW implantation the lid is overloaded and levator muscle needs to continuously overact in order to lift the lid. As the first event that initiates spontaneous blinks are a conjugate bilateral levator
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Maximum Velocity (degree/s)
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200 150 100 50 0 2.5
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normal lid - 6 months
900 800 700 600 500 400 300 200 100
5.0 7.5 10.0 12.5 15.0 17.5 Amplitude (degree)
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15 20 25 Amplitude (degree)
FIGURE 2 Main sequences of a patient with GW implantation. Left, paretic lid; right, normal lid; Top, preoperative data; middle (1 month after surgery, bottom 6 months postoperatively).
TABLE 3 Margin reflex distances and relative amplitudes. GW MPLD (mm) Unaffected lid Paretic lid BL 1m 6m
3.8 ± 0.19 1.8 ± 0.24 2.2 ± 0.25
Mean RA
Autogenous TF sling % RA 41 (95% CI)
1.80 ± 0.04
73.0 (70–76)
0.15 ± 0.004 2.30 ± 0.12 1.80 ± 0.008
0.3 (5.01–1.0) 42.0 (38–46) 47.0 (42–51)
MPLD (mm)
3.8 ± 0.24 2.1 ± 0.32 3.1 ± 0.21
Mean RA
% RA 41 (95% CI)
1.92 ± 0.004
75.6 (72–79)
0.16 ± 0.005 0.76 ± 0.73 0.27 ± 0.01
0.3 (50.01–1.0) 21.0 (17–25) 0.7 (0.2–1.7)
BL, baseline preoperative, 1 m, 1 month; 6 m, 6 months, CI, confidence interval, MPLD, mid-pupil lid distance, RA, relative amplitude.
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Spontaneous Blinking Kinetics on Paralytic Lagophthalmos relaxation, the excessive tension created by the GW lowers the lid margin. Although lid loading procedures with GW are often used11,23–26 there is a relative paucity of data on the effect of this type of surgery on the blink kinematics. Chuke et al. likely were the first to use a magnetic search coil to measure the effect of GW implantation on the blink metrics of one patient with mild orbicularis paresis.27 Two years later Abell et al.13 used magnetic search coil to quantify the blink metrics of six patients who underwent GW implants ranging from 0.8 to 1.8 g. The measurements were performed 8 days after surgery and with variable outcomes.13 The mean preoperative gain (28.6 ± 5.7%) improved to 42.6 ± 7.5%.13 However, the effect was not significant in three patients and high gains (72.1% and 50.0%) were observed in two patients.13 The main sequences were not analyzed but the mean peak velocity of the paretic and contralateral blinks did not change postoperatively.13 A study of 18 patients who had received GW ranging from 0.6 to 1.0 g had their palpebral fissure video-taped for 4 min with a commercial camera.28 Blink amplitudes were calculated as a ratio between the reduction of the palpebral fissure at the end of the closing phase of the blink and before the lid movement. With this method the authors reported that after surgery there was a mean increment of 21.9 ± 19.6% on the blink amplitude. To our knowledge, the effect of autogeneous upper lid cerclage with TF on blink kinematics has not published in English peer review literature. Historically, lid slings were performed with silicone rods as suggested by Arion.9,29 However, due to the high rate of extrusion the Arion surgery was not favored and almost disappeared from the literature. Theoretically, upper lid slings act similarly to GW implantation. The sling creates a continuous passive downward vector that is opposed by levator overaction. When the levator muscle consensually relaxes during a contralateral blink the sling lowers the lid margin. We decided to use TF grafts because this tissue is easily obtained and well tolerated on the upper eyelid. It has used as a sling in temporalis muscle transfer surgeries8,30 and also to drape over GW in order to prevent implant extrusion.31 Although only a small number of subjects were included in this work, we believe that recording a large number of blinks with the magnet search coil, in each subject, revealed interesting information about the eyelid kinetics after upper eyelid GW implant or cerclages in paralytic lagophthalmos. Overall, our results concur well with the only previously published study with the magnetic search coil.13 When the surgeon overloads a paralyzed lid the effect is a modest increase on blink amplitude. In our sample, 6 months postoperatively the mean amplitude of the paretic blinks is just 30% of the amplitude of the !
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contralateral unaffected blinks. The effect with TF slings is similar to the GW but at 6 months there is a decline on the blink gain probably due to material fatigue and loss of fascial tension. Amplitude–velocity relationships are also not affected by increasing the lid load. No significant changes were detected on the main sequence slopes of either the paralyzed or contralateral blinks with GW or TF. These results are somewhat puzzling because there is a clear improvement on eye surface conditions after lid-loading surgery, the corneal keratopathy scores diminished and patients are more comfortable. We think that the positional effect of the surgery in lowering the lid margin is an important factor for favorable outcomes of the procedure. When the lid margin is lowered, the efficacy of the blinks protecting the cornea increases. We have termed this variable as the relative amplitude of blinking. Even if there is no change in the absolute blink amplitude, when the margin reflex distance is reduced the number of blinks that crosses the pupil center augments. Just 1 month after GW implantation the proportion of covering the pupil center increased from 0.3% to 42%. At 6 months postoperatively the MPLD reduction was maintained and so was the relative amplitude of the blinks. With autogenous fascial cerclage these effects almost disappeared with time.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. Grant from Brazilian Research Council (CNPq) #301865/2009-4.
REFERENCES 1. Van de Graaf RC, FF IJ, Nicolai JP. Lagophthalmos or hare eye: an etymologic eye opener. Aesthetic Plast Surg 2008; 32:573–574. 2. Seiff SR, Chang Jr JS. The staged management of ophthalmic complications of facial nerve palsy. Ophthal Plast Reconstr Surg 1993;9:241–249. 3. Muhlbauer WD. [Five years experience with lid magnet implantation for paretic lagophthalmos (author’s transl)]. Klin Monbl Augenheilkd 1977;171:938–945. 4. Morel-Fatio D, Lalardrie JP. Palliative Surgical treatment of facial paralysis. The palpebral spring. Plast Reconstr Surg 1964;33:446–456. 5. Levine RE, Pulec JL. Eyelid reanimation with the palpebral spring after facial nerve graft surgery: an interdisciplinary approach. Ear Nose Throat J 1993;72:686–691. 6. Demirci H, Frueh BR. Palpebral spring in the management of lagophthalmos and exposure keratopathy secondary to facial nerve palsy. Ophthal Plast Reconstr Surg 2009;25: 270–275. 7. Gittins J, Martin K, Sheldrick J, Reddy A, Thean L. Electrical stimulation as a therapeutic option to improve
8
8.
9. 10.
11.
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12.
13.
14.
15. 16.
17.
18.
19.
S. P. Wambier et al. eyelid function in chronic facial nerve disorders. Investig Ophthalmol Vis Sci 1999;40:547–554. Miyamoto S, Takushima A, Okazaki M, Momosawa A, Asato H, Harii K. Retrospective outcome analysis of temporalis muscle transfer for the treatment of paralytic lagophthalmos. J Plast Reconstr Aesthet Surg 2009;62: 1187–1195. Arion HG. Dynamic closure of the lids in paralysis of the orbicularis muscle. Int Surg 1972;57:48–50. Braun T, Batran H, Zengel P, Berghaus A, Hempel JM. Surgical rehabilitation of paralytic lagophthalmus by platinum chain lid loading: focusing on patient benefit and health-related quality of life. Otol Neurotol 2012;33: 1630–1634. Aggarwal E, Naik MN, Honavar SG. Effectiveness of the gold weight trial procedure in predicting the ideal weight for lid loading in facial palsy: a prospective study. Am J Ophthalmol 2007;143:1009–1012. Abenavoli FM, De Gregorio A, Corelli R. Upper eye lid loading with autologous cartilage in paralytic lagophthalmos. Plastic Reconstr Surg 2006;117:2511–2512. Abell KM, Baker RS, Cowen DE, Porter JD. Efficacy of gold weight implants in facial nerve palsy: quantitative alterations in blinking. Vision Res 1998;38:3019–3023. Seiff SR, Sullivan JH, Freeman LN, Ahn J. Pretarsal fixation of gold weights in facial nerve palsy. Ophthal Plast Reconstr Surg 1989;5:104–109. Arion HG. [Technic of dynamic closure of the eyelids in orbicular paralysis]. Ann Chir 1969;23:847–851. McCord CDJ, Codner MA. Facial nerve palsy. Eyelid & periorbital surgery. St Louis, MO: Quality Medical Publishing; 2008. pp. 695–727. Whitnall S. On a tubercle on the malar bone, and on the lateral attachments of the tarsal plates. J Anat Physiol 1911; 45:462–432. Lemp MA. Report of the national eye institute/industry workshop on clinical trials in dry eyes. CLAO J. 1995;21: 221–232. Garcia DM, Barbosa JC, Pinto CT, Cruz AA. Estimation of spontaneous blinking main sequence in normal subjects
20.
21.
22.
23.
24.
25. 26.
27.
28.
29.
30.
31.
and patients with Graves’ upper eyelid retraction. Investig Ophthalmol Vis Sci 2013;54:1434–1442. Huffman MD, Baker RS, Stava MW, Chuke JC, Rouholiman BR, Porter JD. Kinematic analysis of eyelid movements in patients recovering from unilateral facial nerve palsy. Neurology 1996;46:1079–1085. Stava MW, Huffman MD, Baker RS, Epstein AD, Porter JD. Conjugacy of spontaneous blinks in man: eyelid kinematics exhibit bilateral symmetry. Investig Ophthalmol Vis Sci 1994;35:3966–3971. Sibony PA, Evinger C, Manning KA. Eyelid movements in facial paralysis. Arch Ophthalmol 1991;109: 1555–1561. Bladen JC, Norris JH, Malhotra R. Indications and outcomes for revision of gold weight implants in upper eyelid loading. Br J Ophthalmol 2012;96:485–489. Rofagha S, Seiff SR. Long-term results for the use of gold eyelid load weights in the management of facial paralysis. Plast Reconstr Surg 2010;125:142–149. Tower RN, Dailey RA. Gold weight implantation: a better way? Ophthal Plast Reconstr Surg 2004;20:202–206. Yu Y, Sun J, Chen L, Liu L. Lid loading for treatment of paralytic lagophthalmos. Aesthetic Plast Surg 2011;35: 1165–1171. Chuke JC, Baker RS, Porter JD. Bell’s palsy-associated blepharospasm relieved by aiding eyelid closure. Ann Neurol 1996;39:263–268. Terzis JK, Kyere SA. Experience with the gold weight and palpebral spring in the management of paralytic lagophthalmos. Plast Reconstr Surg 2008;121:806–815. English FP, Apel JV. Cerclage technique for dynamic eyelid closure in facial paralysis. Br J Ophthalmol 1973;57: 750–752. Frey M, Giovanoli P, Tzou C-HJ, Kropf N, Friedl S. Dynamic reconstruction of eye closure by muscle transposition or functional muscle transplantation in facial palsy. Plastic Reconstr Surg 2004;114:865–875. Thomas DA, Khalifa YM. Temporalis fascia in the management of gold eyelid weight extrusion. Ophthal Plast Reconstr Surg 2005;21:153–155.
Current Eye Research
Current Eye Research Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/icey20
Spontaneous Blinking Kinetics on Paralytic Lagophthalmos After Lid Load with Gold Weight or Autogenous Temporalis Fascia Sling a
ab
ab
Sarah P. F. Wambier , Denny M. Garcia , Antonio A. V. Cruz
a
& Andre Messias
a
Department of Ophthalmology, Otorhinolaryngology, Head and Neck Surgery, Ribeirão Preto Medical School, University of São Paulo, Sao Paulo, Brazil and b
Craniofacial Research Support Center, University of São Paulo, Sao Paulo, Brazil Published online: 27 May 2015.
Click for updates To cite this article: Sarah P. F. Wambier, Denny M. Garcia, Antonio A. V. Cruz & Andre Messias (2015): Spontaneous Blinking Kinetics on Paralytic Lagophthalmos After Lid Load with Gold Weight or Autogenous Temporalis Fascia Sling, Current Eye Research To link to this article: http://dx.doi.org/10.3109/02713683.2015.1031252
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Current Eye Research, Early Online, 1–8, 2015 ! Informa Healthcare USA, Inc. ISSN: 0271-3683 print / 1460-2202 online DOI: 10.3109/02713683.2015.1031252
ORIGINAL ARTICLE
Spontaneous Blinking Kinetics on Paralytic Lagophthalmos After Lid Load with Gold Weight or Autogenous Temporalis Fascia Sling Sarah P. F. Wambier1, Denny M. Garcia1,2, Antonio A. V. Cruz1,2 and Andre Messias1
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1
Department of Ophthalmology, Otorhinolaryngology, Head and Neck Surgery, Ribeira˜o Preto Medical School, University of Sa˜o Paulo, Sao Paulo, Brazil and 2Craniofacial Research Support Center, University of Sa˜o Paulo, Sao Paulo, Brazil
ABSTRACT Purpose: To assess the upper eyelid kinematics during spontaneous blinking in unilateral paralytic lagophthalmos before and after upper eyelid load with gold weight (GW) or autogenous temporalis fascia (TF) sling. Design: Comparative case series. Subjects: Patients with long-standing unresolved unilateral facial palsy who underwent surgical treatment with GW (n = 8) or upper lid cerclage with TF (n = 10). The contralateral eyelid served as the control for each patient (control group). Methods: Preoperative and postoperative measurements of spontaneous blink kinematics with magnetic search coil and clinical assessment of lid margin position, lagophthalmos and ocular surface exposure, and determine amplitude, maximum velocity and main sequence of spontaneous blinks; relative amplitude of blinks to the pupil center; ocular surface exposure scores; magnitude of lagophthalmos and mid-pupil lid distances. Results: The mean (±SE) down-phase amplitude ratio between paralyzed and contralateral eyelids (blink gain) was 10.0% preoperatively for both groups and significantly increased to 29 ± 6% for the GW group (p50.05) and 23 ± 4% for the TF group (p50.05). At 6 months the gain was significant for the GW group only (32 ± 7%, p50.05). There was no effect on the maximum velocity of the blinks or the main sequence of paretic and contralateral blinks with either surgery. Both procedures lowered the lid margin increasing the number of blinks that reached the pupil center. At 6 months this effect was prominent only for the GW group. Exposure keratopathy scores and lagophthalmos decreased postoperatively especially in the GW group. Conclusions: The beneficial effect of lid load surgeries result from a combination of a small increase on the spontaneous blink amplitude and a static effect due to the reduction of the distance between the lid margin and pupil center. Keywords: Facial palsy, gold weight, lid loading, paralytic lagophthalmos, spontaneous blink, upper eyelid kinematics, upper eyelid sling
INTRODUCTION
believed that hares and rabbits (lagomorph animals) slept with open eyes,1 this term is a pictorial description of the upper lid retraction and poor lid kinetics that accompanies defective upper lid closure.
The word ‘‘lagophthalmos’’ originates from the Greek and literally means hare’s eye.1 As the ancient Greeks
Received 15 September 2014; revised 28 January 2015; accepted 12 March 2015; published online 25 May 2015 Correspondence: Andre Messias, Department of Ophthalmology, Otorhinolaryngology, and Head and Neck Surgery, Ribeira˜o Preto Medical School, University of Sa˜o Paulo, Av. Bandeirantes, 3900, 14049-900 Ribeira˜o Preto, SP, Brazil. Tel: +55 1636022865. Fax: +55 1636022860. E-mail: [email protected]
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S. P. Wambier et al.
Paralytic lagophthalmos occurs when the orbicularis oculi muscle is denervated. In this condition, spontaneous blinks are severely affected and may be virtually absent in cases of complete paresis. The longterm effects of a defective spontaneous blinking activity are devastating for the ocular surface. Exposure keratitis, corneal ulcers and eventually blindness are potential ophthalmic consequences of peripheral facial palsy.2 Restoration of eyelid kinetics in the setting of orbicularis palsy is a difficult problem, which has been addressed by various surgical and non-surgical procedures including the use of magnets,3 springs,4–6 electrical stimulation,7 temporalis muscle transfer,8 eyelid cerclage with silicone bands9 and lid-loading operations.10–12 Although the literature on the different treatment modalities is vast, we are aware of only one study that employed magnetic search coil to quantify the effect of gold weight (GW) implants on spontaneous blink kinetics in six patients.13 In this study, we compared the spontaneous blink metrics after lid loading with GW and upper lid sling with temporalis fascia (TF) on a sample of patients with unresolved facial palsy.
METHODS The study protocol adhered to the tenets of the Declaration of Helsinki and was approved by the local Institutional Review Board. All participants gave written informed consent before entering into the study.
Patients and Groups Eighteen consecutive patients with unilateral irreversible longstanding (mean time = 8 years) facial palsy were enrolled in the study. All patients had grade IV to V facial nerve dysfunction on the House and Brackmman scale with incomplete eye closure and symptoms of eye exposure. The etiologies of the facial palsy were excision of acoustic neuroma or extracranial tumors (n = 13), head trauma (n = 2), congenital (n = 2) and idiopathic (n = 1). Two patients had decreased lacrimal secretion (Schirmer test 55 mm) and one patient had corneal anesthesia. All patients underwent an informed consent that explained the risks and benefits of the surgical procedures. The patients were randomly assigned to undergo either standard pretarsal GW lid procedure (GW group, n = 8) or upper lid sling with TF (TF group, n = 10). The contralateral eyelid served as the control (control group). Both groups had the same gender ratio (1:1). The mean age was 49 years (range, 33–70 years) for the
GW group and 45.9 years for the TF group (range, 27–69 years).
Surgeries In the GW group all patients surgery was performed with a standardized pretarsal fixation of gold implants of 1.0 g (n = 5) or 1.2 g (n = 3) measuring approximately 10 mm length, 5 mm height and 2 mm thickness.14 The TF group underwent a modification of the original Arion technique15 as suggested by McCord and Codner.16 A 30-mm length, 5-mm height strip of TF is removed from the patient’s temporal fossa. A lid crease incision is used to raise a pretarsal skin–muscle flap in order to expose the whole tarsal plate from the upper limb of the medial canthal tendon to lateral insertion of the lateral retinaculum on the lateral orbital rim. The medial end of the fascia is first sutured with non-absorbable suture to the upper limb of the medial canthal tendon. Then, the fascia strip is stretched over the tarsal plate and sutured under tension on the periosteum of the lateral orbital rim at the level of the Whitnall’s tubercle17 creating a strong downward vector on the upper eyelid.
Ophthalmological Examination Preoperatively, and on the first and sixth postoperative months, all patients had a comprehensive ophthalmic examination with special attention to the upper eyelid position, exposure keratopathy and degree of lagophthalmos. Lid margin position relative to the pupil center (mid-pupil lid distance or MPLD) was measured on digital images of the palpebral fissure on primary gaze position with the Image J 1.45 software (National Institute of Health, Bethesda, MD, USA). Digital photography was performed with a Nikon D5000 camera (Nikon Inc., Tokyo, Japan) equipped with a macro Nikkor 60 mm lens. A millimeter ruler was included on the images for pixel/mm conversion. Lagophthalmos was defined as any gap between the upper and lower lids following gentle closure of the fissure. The degree of lagophthalmos was measured with the same equipment used to quantify the MPLDs. Exposure keratopathy was quantified by the degree of corneal staining with fluorescein as described by Lemp.18 The cornea was divided in five areas and a standardized 0–3 system was used for each area of the cornea. The sum of the scores was the keratopathy measurement.
Eyelid Kinematics Recording Spontaneous blinks of both eyes of all patients were registered with the magnetic search coil technique as Current Eye Research
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Spontaneous Blinking Kinetics on Paralytic Lagophthalmos described previously.19 Briefly, subjects were seated comfortably with the head stabilized on a chin rest in a weak magnetic field. Small coils (3.8 mm diameter, 30 turns, 30 mg, copper wire 0.102 mm in diameter) were taped to the center of the pretarsal area of the upper eyelids. The recordings were low-pass filtered at 10 kHz, amplified 20,000 times, digitized with 12-bit precision and sampled at 200 Hz with a computer driven system (Remel Laboratories, San Antonio, TX), that resolved spatial changes in lid rotations as small as 0.18 (equivalent to a linear lid motion of 0.02 mm) every 5 ms. Spontaneous blinks of paretic and contralateral lid were recorded continuously for 5 min, while the subjects watched the same video (commercial movie). Specific software (programmed in C# language) was used to analyze the data. An algorithm based on the derivatives of the blink signal detected the blinks automatically. In addition, the data retrieved were checked manually to avoid mistakes. For each blink, the software calculated the amplitude (degrees) and maximum (peak) velocity ( /s) of the closing phase of the movements. Linear regression was used to fit the main blink sequences (relationship between amplitude and maximum velocity).19 The parameters values of the paretic lid movements were expressed as a percentage of the same parameter of the contralateral normal blinks. This ratio (value of the movement of paretic lid/value of movement of the normal lid) was referred to as blink gain.20 In order to express the lid motion relative to pupil center blink amplitudes were also converted to millimeters according to the well-known formula A = r sin (A0 ), where A is amplitude in mm, r is the radius of the globe (assumed to be 12 mm) and A0 is the amplitude in degrees. The converted amplitudes were then divided by the mid-pupil lid distances. We named this variable ‘‘relative amplitude’’ and blinks with relative amplitude = 1 reached the pupil center. Values 51 and 41 indicate movements, which did not attain or covered the pupil center, respectively.
Statistics Two-way analysis of variances (group across time) with post hoc Tukey–Kramer HSD tests was used to compare the effect of surgery on the degree of lagophthalmos and corneal staining, MPLD, blink kinetics (amplitude, maximum velocity and main sequence) at 1 and 6 months postoperatively. Standard error was used to indicate mean variability throughout the text. All statistical procedures were performed using JMP SAS 11.0 (SAS Institute, Inc., Cary, NC). A p value less than 0.05 was considered statistically significant. !
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RESULTS Eye Surface Scores and Lagophthalmos Measurement The corneal exposure scores were 7.6 ± 1.3 and 7.5 ± 1.4 at baseline, and decreased significantly for both groups over time (F = 24.49, p50.001), to 3.4 ± 0.7 and 1.4 ± 0.5 at 1 month postoperatively, and to 2.8 ± 0.6 and 1.5 ± 0.5 at 6 months postoperatively, for GW and TF groups, respectively. Mean lagophthalmos at baseline was 8.9 ± 0.7 and 8.3 ± 0.7 mm, for the GW and TF groups, respectively, and also decreased significantly postoperatively for both groups (F = 90.14, p50.0001). However, the effect was significantly greater on the GW group (7.73, p = 0.009), which decreased 1.2 ± 0.7 and 3.0 ± 0.9 mm, for GW and TF groups, respectively, 1 month after treatment. The interaction group across time was also significant (F = 4.17, p = 0.025), and at 6 months, lagophthalmos was significantly smaller for GW group: 1.4 ± 0.9 mm, while TF = 3.8 ± 0.8 mm (p50.05 TW group and p40.05 TF group).
Eyelid Kinematics Preoperative spontaneous blink parameters are presented in Table 1. The amplitude of the paretic blinks was less than 20% of the contralateral lids in all but one patient (TF #6). These small blinks were also very slow. The mean slope of relationship between amplitude and maximum velocity was 30% and 48% of the control group for the GW and TF groups, respectively. Blink amplitudes of all paretic lids increased 1 month after lid load with GW (Figure 1), and at 6 months this increase was lost in just one patient, (#7) who showed mean blink gain smaller than preoperatively. High gains were observed in two patients (#4 and #5), and in 50% of the eyes, the amplitude was equal to or greater than 30% of the contralateral lid. In the TF group, the long-term increments of the blink amplitudes were more modest. At 6 months postoperatively, the gains of all cases in the TF group were below 30% and similar to the GW group, in one patient (#5) the gain completely regressed. Mean preoperative amplitude gain (0.10 for both groups) increased to 0.29 ± 0.06 and 0.23 ± 0.04, for GW and FT, respectively, at 1 month postoperatively. ANOVA indicated the factor time was significant (F = 14.23, p50.0001) and the post hoc Tukey test confirmed that, at 6 months postoperatively, the mean gain (0.32 ± 0.07) in the GW group was significantly greater than its baseline value (p = 0.0013), but this effect was not significant in the TF group (0.19 ± 0.03) (p = 0.4538). Table 2 presents the mean values of the main sequence slopes for the paretic and contralateral
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TABLE 1 Preoperative spontaneous blinks parameters for all patients. Paretic eyelid
Group Patient
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GW
1 2 3 4 5 6 7 8
Mean ± SE TF 1 2 3 4 5 6 7 8 9 10 Mean ± SE
N 32 56 177 60 28 255 40 82 91.3 ± 28.9 30 204 32 67 63 34 66 17 29 109 65.1 ± 17.7
Contralateral eyelid
Blink gain (ratio paretic/normal)
Main Main Maximum Main Amplitude Maximum sequence Amplitude Maximum sequence Amplitude velocity sequence velocity ( /s) (1/s) ( ) velocity ( /s) (1/s) ( ) ( /s) (1/s) ( ) 1.6 3.7 2.5 3.7 3.2 2.3 3.7 3.6
58.5 58.5 53.7 62.3 59.5 68.7 65.7 45.7
NS 5.2 6.6 4.8 6.8 5.4 6.8 1.4
27.4 45.0 32.4 44.0 17.9 19.3 25.9 48.8
562.5 877.4 663.7 879.2 261.1 572.9 476.8 1223.4
3.0 ± 0.3 5.6 1.5 2.1 1.6 2.7 4.3 1.0 4.5 3.7 1.4 2.8 ± 0.5
59.1 ± 2.5 58.5 41.2 78.8 66.0 36.4 74.4 21.0 82.5 54.8 30.3 54.4 ± 6.8
5.3 ± 0.7 3.2 5.1 NS 10.3 NS 10.0 7.1 14.2 7.5 11.5 8.6 ± 1.1
32.6 ± 4.3 39.5 41.3 28.9 18.0 25.9 16.4 17.0 50.7 28.9 27.0 29.4 ± 3.6
32.6 13.2 28.3 14.1 17.5 30.9 13.2 22.7
0.06 0.08 0.08 0.08 0.18 0.12 0.14 0.07
689.6 ± 104.8 21.6 ± 2.9 0.10 ± 0.01 772.4 22.0 0.14 999.8 22.5 0.04 768.5 28.9 0.07 505.9 24.4 0.09 447.8 NS 0.10 212.7 6.9 0.26 428.0 28.6 0.06 917.7 44.0 0.09 393.3 NS 0.13 689.7 22.5 0.05 613.6 ± 80.2 25.0 ± 3.3 0.10 ± 0.02
0.10 0.07 0.08 0.07 0.23 0.12 0.14 0.04
– 0.39 0.23 0.34 0.39 0.17 0.52 0.06
0.11 ± 0.02 0.30 ± 0.06 0.08 0.15 0.04 0.23 0.10 – 0.13 0.42 0.08 – 0.35 1.45 0.05 0.25 0.09 0.32 0.14 – 0.04 0.51 0.11 ± 0.03 0.48 ± 0.14
NS, Nonlinear relationships (slopes with p40.05).
blinks before and after surgery. Although slopes of paretic blinks on the TF group were significantly higher than in the GW (F = 5.91, p = 0.03), neither the factor time (paretic F = 1.56, p = 0.23, contralateral F = 0.47, p = 0.63) nor the interaction time versus group (paretic F = 0.16, p = 0.86, contralateral F = 1.81, p = 0.18) was significant for both lids. Figure 2 shows an example of the stability of the main sequence of the paretic and normal lid. The relative amplitude of the blinks is dependent on the values of blink amplitude and the static position of the lid. As shown in Table 3, the mean MPLD decreased on the first postoperative month on both groups (p50.001), but at 6 months this MPLD was not significantly different from baseline for the TF group (p = 0.2520). The diminished effect of the FT on MPLD with time coupled with the smaller blink gain induced by the surgery explains the striking difference between the groups regarding the relative amplitude of the blinks. At 6 months postoperatively, 47% of the blinks in the GW group had amplitudes large enough to cover the pupil center while only of 0.7% blinks from the lids in the TF group had the same level of effectiveness. As expected, the mean relative amplitude of the GW group was statistically significantly greater than baseline at 1 month postoperatively (p = 0.0186), and showed statistical significance at 6 months (p = 0.05), but this effect was not observed for the TF group (1 month: p = 0.6777; 6 months: p = 0.9887).
DISCUSSION Spontaneous blinks are highly conjugate bilateral movements. In normal subjects the variability in amplitude between eyes is narrow with gains ranging from 0.8 to 1.2. Acute orbicularis palsy introduces an abrupt asymmetry to blinking. As the innervation to the orbicularis muscle is suppressed, the active force that generates the closing phase of the blinks disappears and the only forces capable of lowering the paretic eyelid margin are those generated by the relaxation of the levator palpebral superioris muscle.21 Our results concur with previous observations that in severe long-standing unresolved orbicularis palsy, the abnormal blinks observed in the affected lids represent passive movements.20 In general, these blinks have small amplitudes (in our sample the mean gain was just 0.1) and low velocity–amplitude relationships. Notably, although the range of amplitude of the paretic blinks was limited, only 16.7% of their main sequences could not be fitted by linear regression lines. In all but one case, the slopes of these main sequences were less than half of the slopes of the contralateral (control) lids. The blink metrics of the unaffected lids were all within the normal range.19 This finding confirms previous suggestions that compensatory hyperactive phenomena, seen in the unaffected lids of patients with mild facial palsy,22 are not recruited when the facial palsy is severe. Current Eye Research
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FIGURE 1 Effect of gold weigh (top) and upper eyelid TF cerclage (bottom) on the gain of spontaneous blink amplitude. Baseline preoperative values (BL) and postoperative changes at one (1M) and six months (6M).
TABLE 2 Mean slopes of the main sequence (1/s). Paretic lid BL
1m
Normal lid 6m
BL
1m
6m
GW 5.3 ± 0.7 6.6 ± 1.0 7.2 ± 1.0 21.6 ± 2.9 22.7 ± 2.9 24.3 ± 3.3 TF 8.6 ± 1.1 8.9 ± 1.0 10.0 ± 1.4 25.0 ± 3.3 18.7 ± 3.0 18.6 ± 2.3
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The most common treatment modalities of paralytic lagophthalmos are based on the increment of the passive eyelid forces stored by the elastic components of the lid. With GW implantation the lid is overloaded and levator muscle needs to continuously overact in order to lift the lid. As the first event that initiates spontaneous blinks are a conjugate bilateral levator
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FIGURE 2 Main sequences of a patient with GW implantation. Left, paretic lid; right, normal lid; Top, preoperative data; middle (1 month after surgery, bottom 6 months postoperatively).
TABLE 3 Margin reflex distances and relative amplitudes. GW MPLD (mm) Unaffected lid Paretic lid BL 1m 6m
3.8 ± 0.19 1.8 ± 0.24 2.2 ± 0.25
Mean RA
Autogenous TF sling % RA 41 (95% CI)
1.80 ± 0.04
73.0 (70–76)
0.15 ± 0.004 2.30 ± 0.12 1.80 ± 0.008
0.3 (5.01–1.0) 42.0 (38–46) 47.0 (42–51)
MPLD (mm)
3.8 ± 0.24 2.1 ± 0.32 3.1 ± 0.21
Mean RA
% RA 41 (95% CI)
1.92 ± 0.004
75.6 (72–79)
0.16 ± 0.005 0.76 ± 0.73 0.27 ± 0.01
0.3 (50.01–1.0) 21.0 (17–25) 0.7 (0.2–1.7)
BL, baseline preoperative, 1 m, 1 month; 6 m, 6 months, CI, confidence interval, MPLD, mid-pupil lid distance, RA, relative amplitude.
Current Eye Research
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Spontaneous Blinking Kinetics on Paralytic Lagophthalmos relaxation, the excessive tension created by the GW lowers the lid margin. Although lid loading procedures with GW are often used11,23–26 there is a relative paucity of data on the effect of this type of surgery on the blink kinematics. Chuke et al. likely were the first to use a magnetic search coil to measure the effect of GW implantation on the blink metrics of one patient with mild orbicularis paresis.27 Two years later Abell et al.13 used magnetic search coil to quantify the blink metrics of six patients who underwent GW implants ranging from 0.8 to 1.8 g. The measurements were performed 8 days after surgery and with variable outcomes.13 The mean preoperative gain (28.6 ± 5.7%) improved to 42.6 ± 7.5%.13 However, the effect was not significant in three patients and high gains (72.1% and 50.0%) were observed in two patients.13 The main sequences were not analyzed but the mean peak velocity of the paretic and contralateral blinks did not change postoperatively.13 A study of 18 patients who had received GW ranging from 0.6 to 1.0 g had their palpebral fissure video-taped for 4 min with a commercial camera.28 Blink amplitudes were calculated as a ratio between the reduction of the palpebral fissure at the end of the closing phase of the blink and before the lid movement. With this method the authors reported that after surgery there was a mean increment of 21.9 ± 19.6% on the blink amplitude. To our knowledge, the effect of autogeneous upper lid cerclage with TF on blink kinematics has not published in English peer review literature. Historically, lid slings were performed with silicone rods as suggested by Arion.9,29 However, due to the high rate of extrusion the Arion surgery was not favored and almost disappeared from the literature. Theoretically, upper lid slings act similarly to GW implantation. The sling creates a continuous passive downward vector that is opposed by levator overaction. When the levator muscle consensually relaxes during a contralateral blink the sling lowers the lid margin. We decided to use TF grafts because this tissue is easily obtained and well tolerated on the upper eyelid. It has used as a sling in temporalis muscle transfer surgeries8,30 and also to drape over GW in order to prevent implant extrusion.31 Although only a small number of subjects were included in this work, we believe that recording a large number of blinks with the magnet search coil, in each subject, revealed interesting information about the eyelid kinetics after upper eyelid GW implant or cerclages in paralytic lagophthalmos. Overall, our results concur well with the only previously published study with the magnetic search coil.13 When the surgeon overloads a paralyzed lid the effect is a modest increase on blink amplitude. In our sample, 6 months postoperatively the mean amplitude of the paretic blinks is just 30% of the amplitude of the !
2015 Informa Healthcare USA, Inc.
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contralateral unaffected blinks. The effect with TF slings is similar to the GW but at 6 months there is a decline on the blink gain probably due to material fatigue and loss of fascial tension. Amplitude–velocity relationships are also not affected by increasing the lid load. No significant changes were detected on the main sequence slopes of either the paralyzed or contralateral blinks with GW or TF. These results are somewhat puzzling because there is a clear improvement on eye surface conditions after lid-loading surgery, the corneal keratopathy scores diminished and patients are more comfortable. We think that the positional effect of the surgery in lowering the lid margin is an important factor for favorable outcomes of the procedure. When the lid margin is lowered, the efficacy of the blinks protecting the cornea increases. We have termed this variable as the relative amplitude of blinking. Even if there is no change in the absolute blink amplitude, when the margin reflex distance is reduced the number of blinks that crosses the pupil center augments. Just 1 month after GW implantation the proportion of covering the pupil center increased from 0.3% to 42%. At 6 months postoperatively the MPLD reduction was maintained and so was the relative amplitude of the blinks. With autogenous fascial cerclage these effects almost disappeared with time.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. Grant from Brazilian Research Council (CNPq) #301865/2009-4.
REFERENCES 1. Van de Graaf RC, FF IJ, Nicolai JP. Lagophthalmos or hare eye: an etymologic eye opener. Aesthetic Plast Surg 2008; 32:573–574. 2. Seiff SR, Chang Jr JS. The staged management of ophthalmic complications of facial nerve palsy. Ophthal Plast Reconstr Surg 1993;9:241–249. 3. Muhlbauer WD. [Five years experience with lid magnet implantation for paretic lagophthalmos (author’s transl)]. Klin Monbl Augenheilkd 1977;171:938–945. 4. Morel-Fatio D, Lalardrie JP. Palliative Surgical treatment of facial paralysis. The palpebral spring. Plast Reconstr Surg 1964;33:446–456. 5. Levine RE, Pulec JL. Eyelid reanimation with the palpebral spring after facial nerve graft surgery: an interdisciplinary approach. Ear Nose Throat J 1993;72:686–691. 6. Demirci H, Frueh BR. Palpebral spring in the management of lagophthalmos and exposure keratopathy secondary to facial nerve palsy. Ophthal Plast Reconstr Surg 2009;25: 270–275. 7. Gittins J, Martin K, Sheldrick J, Reddy A, Thean L. Electrical stimulation as a therapeutic option to improve
8
8.
9. 10.
11.
Downloaded by [New York University] at 03:03 02 September 2015
12.
13.
14.
15. 16.
17.
18.
19.
S. P. Wambier et al. eyelid function in chronic facial nerve disorders. Investig Ophthalmol Vis Sci 1999;40:547–554. Miyamoto S, Takushima A, Okazaki M, Momosawa A, Asato H, Harii K. Retrospective outcome analysis of temporalis muscle transfer for the treatment of paralytic lagophthalmos. J Plast Reconstr Aesthet Surg 2009;62: 1187–1195. Arion HG. Dynamic closure of the lids in paralysis of the orbicularis muscle. Int Surg 1972;57:48–50. Braun T, Batran H, Zengel P, Berghaus A, Hempel JM. Surgical rehabilitation of paralytic lagophthalmus by platinum chain lid loading: focusing on patient benefit and health-related quality of life. Otol Neurotol 2012;33: 1630–1634. Aggarwal E, Naik MN, Honavar SG. Effectiveness of the gold weight trial procedure in predicting the ideal weight for lid loading in facial palsy: a prospective study. Am J Ophthalmol 2007;143:1009–1012. Abenavoli FM, De Gregorio A, Corelli R. Upper eye lid loading with autologous cartilage in paralytic lagophthalmos. Plastic Reconstr Surg 2006;117:2511–2512. Abell KM, Baker RS, Cowen DE, Porter JD. Efficacy of gold weight implants in facial nerve palsy: quantitative alterations in blinking. Vision Res 1998;38:3019–3023. Seiff SR, Sullivan JH, Freeman LN, Ahn J. Pretarsal fixation of gold weights in facial nerve palsy. Ophthal Plast Reconstr Surg 1989;5:104–109. Arion HG. [Technic of dynamic closure of the eyelids in orbicular paralysis]. Ann Chir 1969;23:847–851. McCord CDJ, Codner MA. Facial nerve palsy. Eyelid & periorbital surgery. St Louis, MO: Quality Medical Publishing; 2008. pp. 695–727. Whitnall S. On a tubercle on the malar bone, and on the lateral attachments of the tarsal plates. J Anat Physiol 1911; 45:462–432. Lemp MA. Report of the national eye institute/industry workshop on clinical trials in dry eyes. CLAO J. 1995;21: 221–232. Garcia DM, Barbosa JC, Pinto CT, Cruz AA. Estimation of spontaneous blinking main sequence in normal subjects
20.
21.
22.
23.
24.
25. 26.
27.
28.
29.
30.
31.
and patients with Graves’ upper eyelid retraction. Investig Ophthalmol Vis Sci 2013;54:1434–1442. Huffman MD, Baker RS, Stava MW, Chuke JC, Rouholiman BR, Porter JD. Kinematic analysis of eyelid movements in patients recovering from unilateral facial nerve palsy. Neurology 1996;46:1079–1085. Stava MW, Huffman MD, Baker RS, Epstein AD, Porter JD. Conjugacy of spontaneous blinks in man: eyelid kinematics exhibit bilateral symmetry. Investig Ophthalmol Vis Sci 1994;35:3966–3971. Sibony PA, Evinger C, Manning KA. Eyelid movements in facial paralysis. Arch Ophthalmol 1991;109: 1555–1561. Bladen JC, Norris JH, Malhotra R. Indications and outcomes for revision of gold weight implants in upper eyelid loading. Br J Ophthalmol 2012;96:485–489. Rofagha S, Seiff SR. Long-term results for the use of gold eyelid load weights in the management of facial paralysis. Plast Reconstr Surg 2010;125:142–149. Tower RN, Dailey RA. Gold weight implantation: a better way? Ophthal Plast Reconstr Surg 2004;20:202–206. Yu Y, Sun J, Chen L, Liu L. Lid loading for treatment of paralytic lagophthalmos. Aesthetic Plast Surg 2011;35: 1165–1171. Chuke JC, Baker RS, Porter JD. Bell’s palsy-associated blepharospasm relieved by aiding eyelid closure. Ann Neurol 1996;39:263–268. Terzis JK, Kyere SA. Experience with the gold weight and palpebral spring in the management of paralytic lagophthalmos. Plast Reconstr Surg 2008;121:806–815. English FP, Apel JV. Cerclage technique for dynamic eyelid closure in facial paralysis. Br J Ophthalmol 1973;57: 750–752. Frey M, Giovanoli P, Tzou C-HJ, Kropf N, Friedl S. Dynamic reconstruction of eye closure by muscle transposition or functional muscle transplantation in facial palsy. Plastic Reconstr Surg 2004;114:865–875. Thomas DA, Khalifa YM. Temporalis fascia in the management of gold eyelid weight extrusion. Ophthal Plast Reconstr Surg 2005;21:153–155.
Current Eye Research
