Graefes Arch Clin Exp Ophthalmol DOI 10.1007/s00417-017-3792-9
OCULOPLASTICS AND ORBIT
Bell’s phenomenon in thyroid-associated inferior rectus myopathy Yasuhiro Takahashi 1 & Maria Suzanne Sabundayo 1 & Hidenori Mito 2 & Hidetaka Miyazaki 3 & Hirohiko Kakizaki 1
Received: 22 May 2017 / Revised: 24 July 2017 / Accepted: 22 August 2017 # Springer-Verlag GmbH Germany 2017
Abstract Purpose To examine Bell’s phenomenon in patients with unilateral thyroid-associated inferior rectus myopathy and changes in this phenomenon after inferior rectus muscle recession. Methods This prospective interventional study included 12 patients who underwent inferior rectus muscle recession with or without nasal transposition. Bell’s phenomenon was examined before and 3 months after surgery. The upper eyelid was held open by a finger to prevent complete eyelid closure. Then, the distance of upward excursion of the inferior corneal limbus or the corneal light reflex was measured during voluntary maximum forced eyelid closure. The pre- and postoperative distances of upward excursion on the affected side were statistically compared with the preoperative distance on the unaffected side using the Mann-Whitney U test, and the preand postoperative distances on the affected side were statistically compared using paired t-test. The relationships among postoperative changes of Bell’s phenomenon, patient age, the amount of recession and nasal transposition of the inferior rectus muscle, postoperative angle of ocular deviation, and reduction in the angle after surgery were analyzed using stepwise multiple regression analyses.
* Yasuhiro Takahashi [email protected]
1
Department of Oculoplastic, Orbital and Lacrimal Surgery, Aichi Medical University Hospital, 1-1 Yazako-Karimata, Nagakute, Aichi 480-1195, Japan
2
Ide Eye Hospital, Yamagata, Japan
3
Department of Plastic and Reconstructive Surgery, Wakayama Medical University, Wakayama, Japan
Results The preoperative measurement of Bell’s phenomenon was significantly shorter on the affected side (1.6 ± 1.6 mm) than the unaffected side (4.3 ± 1.6 mm; P = 0.001). However, the distance on the affected side significantly increased after surgery (4.1 ± 1.9 mm; P < 0.001), compared to the preoperative distance on the unaffected side (P = 0.843). Using a stepwise method, all variables were deleted from the regression equation. Conclusions Bell’s phenomenon decreased on the affected side, which improved after inferior rectus muscle recession. Keywords Bell’s phenomenon . thyroid-associated inferior rectus myopathy . inferior rectus muscle recession . nasal transposition of the inferior rectus muscle
Introduction Bell’s phenomenon is a normal defense reflex in which the eye moves upward and outward during attempted eyelid closure [1]. It can be observed during incomplete blinking, but is also present behind forcibly closed eyelids in normal individuals [1]. Bell’s phenomenon prevents corneal desiccation by means of the upper eyelid covering the cornea in patients with lagophthalmos [2]. The inferior rectus muscle is occasionally inflamed in patients with thyroid eye disease [3]. Subsequent fibrotic changes in the inferior rectus muscle cause hypotropia with limited elevation of the eye, for which recession of the muscle is the primary treatment [3]. Bell’s phenomenon is, therefore, presumed to decrease in patients with inferior rectus myopathy and improve after inferior rectus muscle recession. A previous report briefly mentioned impairment of Bell’s phenomenon in patients with thyroid eye disease [4]; however, none of the previous studies have clarified this notion.
Graefes Arch Clin Exp Ophthalmol
Here, we examined Bell’s phenomenon in patients with thyroid-associated inferior rectus myopathy and changes in Bell’s phenomenon after inferior rectus muscle recession.
Materials and methods Study design, patients, and ethics approval This study was a prospective, interventional study, which included patients diagnosed with thyroid-associated inferior rectus myopathy and underwent inferior rectus muscle recession with or without nasal transposition for correction of diplopia in the primary position at Aichi Medical University Hospital between February 2016 and February 2017 by two authors (YT and HK). Thyroid-associated inferior rectus myopathy was diagnosed by the presence of restrictive hypotropia [5] and a thickened inferior rectus muscle on coronal magnetic resonance imaging (> 5.5 mm of thickness [mean value + 2 × standard deviation, examined in a normal Asian population, reported in a previous report]) [6]. All patients showed unilateral inferior rectus myopathy with normal thickness of all the other extraocular muscles on both eyes as seen on coronal magnetic resonance images [6]. None of the patients had a history of neurologic diseases [7] or orbital decompression surgery. This study was approved by the Institutional Review Board at Aichi Medical University Hospital (approval number, 16H153) and adhered to the tenets of the 1964 Declaration of Helsinki and its later amendments. This study was registered at University Hospital Medical Information Network (identification number, UMIN000026236). Informed consent was provided by all patients for their information to be used in research. Informed consent was also obtained from the patients for publication of any accompanying images. Data collection The following patient data were collected: sex, age, laterality, the presence or absence of lagophthalmos and lower eyelid retraction, angle of ocular deviation measured using a synoptophore [3, 8], the amount of recession and nasal transposition of the inferior rectus muscle, and corneal condition. The presence of lower eyelid retraction was defined when the lower eyelid margin was located below the inferior corneal limbus [9]. Bell’s phenomenon was examined before and 3 months after surgery. As we desired to mainly examine the relationship between thyroid-associated inferior rectus myopathy, lagophthalmos, corneal condition, and eye movement during eyelid closure, we only measured the upward excursion of the eye during eyelid closure. During the examinations, the upper eyelid was held open by a finger to prevent complete eyelid closure. Then, the distance of upward excursion of the inferior
corneal limbus or the corneal light reflex was measured during voluntary maximum forced eyelid closure using a ruler (Fig. 1). The condition of the cornea was evaluated before and 3 months after surgery using the area (A) and density (D) classification of corneal fluorescein staining [10]. A was classified as follows: no punctate staining (A0); punctate staining involving less than one third (A1), one third to two thirds (A2), or more than two thirds of the cornea (A3). D was classified as follows: no punctate staining (D0); sparse (D1), moderate (D2), or high density with overlapped lesions (D3). All examinations were performed by one of the authors (YT). Surgical technique Surgery was performed under general anaesthesia. A perilimbal conjunctival incision, with radial relaxing incisions, was made in the inferior quadrant. A muscle hook was used to secure the inferior rectus muscle at its insertion, and the Tenon’s capsule around the inferior rectus muscle was thoroughly dissected using cotton swabs. As the tendon width varies among individuals [11], the width of the inferior rectus muscle tendon was measured at the scleral insertion using a caliper. The inferior rectus muscle tendon was secured using locking sutures at two points 1 mm posterior to the globe insertion, because the tip thickness of the muscle hook was 1 mm. Next, the inferior rectus muscle was detached from its insertion. In patients with simple inferior muscle recession, the sutures were fixed to the sclera 1 mm posterior to the point that was estimated on the basis of the preoperative ocular deviation angle. Recession of the inferior rectus muscle was calculated as follows: 2° of ocular deviation per 1 mm inferior rectus muscle recession [3]. We managed to leave a residual hypotropia of 3-4° for reading. In patients with both inferior rectus muscle recession and nasal inferior rectus muscle transposition, the inferior rectus muscle was transposed nasally along the spiral of Tillaux; this was concomitantly done with inferior rectus muscle recession. The amount of nasal inferior rectus muscle transposition was preoperatively calculated based on the preoperative deviation angle and the measurement result of the tendon width as follows: 8° of ocular deviation per one inferior rectus muscle tendon width transposition [8]. The inferior rectus muscle tendon was additionally secured to the sclera at one to four points to prevent slippage of the inferior rectus muscle. Finally, the conjunctiva was closed. Lower eyelid retractor lysis or Lockwood ligament advancement were not performed in any of the surgeries [12] because we always plan any contemplated eyelid surgery 6 months after strabismus surgery [5]. Statistical analyses Patient age, the amount of inferior rectus muscle recession and nasal transposition, and the distance of upward excursion of
Graefes Arch Clin Exp Ophthalmol Fig. 1 Bell’s phenomenon. Elevation of the eye during eyelid closure with the upper eyelid being held. (a) and (b) Preoperative patient photos. (a) Before eyelid closure. (b) During eyelid closure. (c) and (d) Postoperative patient photos. (c) Before eyelid closure. (d) During eyelid closure.
the inferior corneal limbus or the corneal light reflex were expressed as means ± standard deviations. The pre- and postoperative distances of upward excursion on the affected side were statistically compared with the preoperative distance on the unaffected side using the Mann-Whitney U test. The preand postoperative distances on the affected side were statistically compared using paired t-test . The relationship among postoperative changes in Bell’s phenomenon, patient age, the amount of recession and nasal transposition of the inferior rectus muscle, postoperative angle of ocular deviation, and reduction in the angle after surgery were analyzed using stepwise multiple regression analyses. The scores of BA^ and BD^ were compared before and after surgery using the Wilcoxon signed-rank test. All statistical analyses were performed using SPSS™ version 22 software (IBM Japan, Tokyo, Japan). A P value of
OCULOPLASTICS AND ORBIT
Bell’s phenomenon in thyroid-associated inferior rectus myopathy Yasuhiro Takahashi 1 & Maria Suzanne Sabundayo 1 & Hidenori Mito 2 & Hidetaka Miyazaki 3 & Hirohiko Kakizaki 1
Received: 22 May 2017 / Revised: 24 July 2017 / Accepted: 22 August 2017 # Springer-Verlag GmbH Germany 2017
Abstract Purpose To examine Bell’s phenomenon in patients with unilateral thyroid-associated inferior rectus myopathy and changes in this phenomenon after inferior rectus muscle recession. Methods This prospective interventional study included 12 patients who underwent inferior rectus muscle recession with or without nasal transposition. Bell’s phenomenon was examined before and 3 months after surgery. The upper eyelid was held open by a finger to prevent complete eyelid closure. Then, the distance of upward excursion of the inferior corneal limbus or the corneal light reflex was measured during voluntary maximum forced eyelid closure. The pre- and postoperative distances of upward excursion on the affected side were statistically compared with the preoperative distance on the unaffected side using the Mann-Whitney U test, and the preand postoperative distances on the affected side were statistically compared using paired t-test. The relationships among postoperative changes of Bell’s phenomenon, patient age, the amount of recession and nasal transposition of the inferior rectus muscle, postoperative angle of ocular deviation, and reduction in the angle after surgery were analyzed using stepwise multiple regression analyses.
* Yasuhiro Takahashi [email protected]
1
Department of Oculoplastic, Orbital and Lacrimal Surgery, Aichi Medical University Hospital, 1-1 Yazako-Karimata, Nagakute, Aichi 480-1195, Japan
2
Ide Eye Hospital, Yamagata, Japan
3
Department of Plastic and Reconstructive Surgery, Wakayama Medical University, Wakayama, Japan
Results The preoperative measurement of Bell’s phenomenon was significantly shorter on the affected side (1.6 ± 1.6 mm) than the unaffected side (4.3 ± 1.6 mm; P = 0.001). However, the distance on the affected side significantly increased after surgery (4.1 ± 1.9 mm; P < 0.001), compared to the preoperative distance on the unaffected side (P = 0.843). Using a stepwise method, all variables were deleted from the regression equation. Conclusions Bell’s phenomenon decreased on the affected side, which improved after inferior rectus muscle recession. Keywords Bell’s phenomenon . thyroid-associated inferior rectus myopathy . inferior rectus muscle recession . nasal transposition of the inferior rectus muscle
Introduction Bell’s phenomenon is a normal defense reflex in which the eye moves upward and outward during attempted eyelid closure [1]. It can be observed during incomplete blinking, but is also present behind forcibly closed eyelids in normal individuals [1]. Bell’s phenomenon prevents corneal desiccation by means of the upper eyelid covering the cornea in patients with lagophthalmos [2]. The inferior rectus muscle is occasionally inflamed in patients with thyroid eye disease [3]. Subsequent fibrotic changes in the inferior rectus muscle cause hypotropia with limited elevation of the eye, for which recession of the muscle is the primary treatment [3]. Bell’s phenomenon is, therefore, presumed to decrease in patients with inferior rectus myopathy and improve after inferior rectus muscle recession. A previous report briefly mentioned impairment of Bell’s phenomenon in patients with thyroid eye disease [4]; however, none of the previous studies have clarified this notion.
Graefes Arch Clin Exp Ophthalmol
Here, we examined Bell’s phenomenon in patients with thyroid-associated inferior rectus myopathy and changes in Bell’s phenomenon after inferior rectus muscle recession.
Materials and methods Study design, patients, and ethics approval This study was a prospective, interventional study, which included patients diagnosed with thyroid-associated inferior rectus myopathy and underwent inferior rectus muscle recession with or without nasal transposition for correction of diplopia in the primary position at Aichi Medical University Hospital between February 2016 and February 2017 by two authors (YT and HK). Thyroid-associated inferior rectus myopathy was diagnosed by the presence of restrictive hypotropia [5] and a thickened inferior rectus muscle on coronal magnetic resonance imaging (> 5.5 mm of thickness [mean value + 2 × standard deviation, examined in a normal Asian population, reported in a previous report]) [6]. All patients showed unilateral inferior rectus myopathy with normal thickness of all the other extraocular muscles on both eyes as seen on coronal magnetic resonance images [6]. None of the patients had a history of neurologic diseases [7] or orbital decompression surgery. This study was approved by the Institutional Review Board at Aichi Medical University Hospital (approval number, 16H153) and adhered to the tenets of the 1964 Declaration of Helsinki and its later amendments. This study was registered at University Hospital Medical Information Network (identification number, UMIN000026236). Informed consent was provided by all patients for their information to be used in research. Informed consent was also obtained from the patients for publication of any accompanying images. Data collection The following patient data were collected: sex, age, laterality, the presence or absence of lagophthalmos and lower eyelid retraction, angle of ocular deviation measured using a synoptophore [3, 8], the amount of recession and nasal transposition of the inferior rectus muscle, and corneal condition. The presence of lower eyelid retraction was defined when the lower eyelid margin was located below the inferior corneal limbus [9]. Bell’s phenomenon was examined before and 3 months after surgery. As we desired to mainly examine the relationship between thyroid-associated inferior rectus myopathy, lagophthalmos, corneal condition, and eye movement during eyelid closure, we only measured the upward excursion of the eye during eyelid closure. During the examinations, the upper eyelid was held open by a finger to prevent complete eyelid closure. Then, the distance of upward excursion of the inferior
corneal limbus or the corneal light reflex was measured during voluntary maximum forced eyelid closure using a ruler (Fig. 1). The condition of the cornea was evaluated before and 3 months after surgery using the area (A) and density (D) classification of corneal fluorescein staining [10]. A was classified as follows: no punctate staining (A0); punctate staining involving less than one third (A1), one third to two thirds (A2), or more than two thirds of the cornea (A3). D was classified as follows: no punctate staining (D0); sparse (D1), moderate (D2), or high density with overlapped lesions (D3). All examinations were performed by one of the authors (YT). Surgical technique Surgery was performed under general anaesthesia. A perilimbal conjunctival incision, with radial relaxing incisions, was made in the inferior quadrant. A muscle hook was used to secure the inferior rectus muscle at its insertion, and the Tenon’s capsule around the inferior rectus muscle was thoroughly dissected using cotton swabs. As the tendon width varies among individuals [11], the width of the inferior rectus muscle tendon was measured at the scleral insertion using a caliper. The inferior rectus muscle tendon was secured using locking sutures at two points 1 mm posterior to the globe insertion, because the tip thickness of the muscle hook was 1 mm. Next, the inferior rectus muscle was detached from its insertion. In patients with simple inferior muscle recession, the sutures were fixed to the sclera 1 mm posterior to the point that was estimated on the basis of the preoperative ocular deviation angle. Recession of the inferior rectus muscle was calculated as follows: 2° of ocular deviation per 1 mm inferior rectus muscle recession [3]. We managed to leave a residual hypotropia of 3-4° for reading. In patients with both inferior rectus muscle recession and nasal inferior rectus muscle transposition, the inferior rectus muscle was transposed nasally along the spiral of Tillaux; this was concomitantly done with inferior rectus muscle recession. The amount of nasal inferior rectus muscle transposition was preoperatively calculated based on the preoperative deviation angle and the measurement result of the tendon width as follows: 8° of ocular deviation per one inferior rectus muscle tendon width transposition [8]. The inferior rectus muscle tendon was additionally secured to the sclera at one to four points to prevent slippage of the inferior rectus muscle. Finally, the conjunctiva was closed. Lower eyelid retractor lysis or Lockwood ligament advancement were not performed in any of the surgeries [12] because we always plan any contemplated eyelid surgery 6 months after strabismus surgery [5]. Statistical analyses Patient age, the amount of inferior rectus muscle recession and nasal transposition, and the distance of upward excursion of
Graefes Arch Clin Exp Ophthalmol Fig. 1 Bell’s phenomenon. Elevation of the eye during eyelid closure with the upper eyelid being held. (a) and (b) Preoperative patient photos. (a) Before eyelid closure. (b) During eyelid closure. (c) and (d) Postoperative patient photos. (c) Before eyelid closure. (d) During eyelid closure.
the inferior corneal limbus or the corneal light reflex were expressed as means ± standard deviations. The pre- and postoperative distances of upward excursion on the affected side were statistically compared with the preoperative distance on the unaffected side using the Mann-Whitney U test. The preand postoperative distances on the affected side were statistically compared using paired t-test . The relationship among postoperative changes in Bell’s phenomenon, patient age, the amount of recession and nasal transposition of the inferior rectus muscle, postoperative angle of ocular deviation, and reduction in the angle after surgery were analyzed using stepwise multiple regression analyses. The scores of BA^ and BD^ were compared before and after surgery using the Wilcoxon signed-rank test. All statistical analyses were performed using SPSS™ version 22 software (IBM Japan, Tokyo, Japan). A P value of
