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Electrical activity of the orbicularis muscles before and after installation of ocular prostheses
Int. J. Oral Maxillofac. Surg. 2015; 44: 127–131 http://dx.doi.org/10.1016/j.ijom.2014.09.021, available online at http://www.sciencedirect.com
Clinical Paper Clinical Pathology
Electrical activity of the orbicularis muscles before and after installation of ocular prostheses
M. C. Goiato, M. R. Santos, B. C. Z. Monteiro, A. Moreno, L. C. Bannwart, A. J. V. Filho, A. M. Guiotti, M. F. Haddad, A. A. Pesqueira, D. M. dos Santos Oral Oncology Centre, School of Dentistry of Arac¸atuba, UNESP, Universidade Estadual Paulista, Arac¸atuba, Sa˜o Paulo, Brazil
M. C. Goiato, M. R. Santos, B. C. Z. Monteiro, A. Moreno, L. C. Bannwart, A. J. V. Filho, A. M. Guiotti, M. F. Haddad, A. A. Pesqueira, D. M. dos Santos: Electrical activity of the orbicularis muscles before and after installation of ocular prostheses. Int. J. Oral Maxillofac. Surg. 2015; 44: 127–131. # 2014 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Abstract. This study examined the electrical activity of the superior (SO) and inferior (IO) orbicularis oculi muscles before and after installing ocular prostheses in patients who had undergone unilateral enucleation. Twelve volunteers requiring prostheses were selected. Their electrical activity was monitored at rest and during normal opening and closing of the eyelids, rapid opening and closing of the eyelids, and squeezing. Data were recorded before and 7, 30, and 60 days after the ocular prosthesis was installed. Two-way analysis of variance was performed to verify whether there were any significant differences between the muscles and periods, and means were compared by Tukey–Kramer honestly significant difference (HSD) tests (P < 0.05). Results from the initial period differed significantly from those after prosthesis installation in all clinical situations. The SO had significantly higher electrical activity levels than the IO in all clinical situations but squeezing. The authors observed the same values during the initial period for the condition of rest (SO 8.42/IO 5.93) and the highest values for the condition of squeezing after 60 days (SO 131.50/IO 117.12). Rehabilitative treatment promoted an increase in the electrical activity of the orbicularis oculi muscles, restoring part of the muscle tone and motor function to muscles of the affected area.
Orbital defects are embarrassing to patients because they affect the face, which is essential to human relationships.1–3 The absence of an ocular globe can lead to atrophy of the orbicularis muscles of the eye, thereby altering the muscle tone of the facial area.4,5 The 0901-5027/010127 + 05
palpebral cutaneous musculature is of supreme importance to facial appearance and expression, and it protects the ocular cavities.6–8 Three ocular–orbital–palpebral surgeries are related to ocular bulb removal: evisceration, comprising the partial removal of the ocular bulb with
Key words: eye enucleation; eye; artificial; electromyography. Accepted for publication 19 September 2014 Available online 3 November 2014
conservation of the sclera; enucleation, comprising the total removal of the bulb with only the capsule and oculomotor muscles remaining; and exenteration, comprising the removal of all contents of the orbital cavity and the circumjacent tissue.9–14
# 2014 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
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To rehabilitate patients with deformities of the ocular bulb, an ocular prosthesis may be used.15–20 Prosthesis use improves the patient’s aesthetic appearance, helping their psychosocial development and improving their quality of life.1–3 The prosthesis does not restore the original function of vision, but it keeps the anophthalmic cavity filled, restoring lacrimal direction and preventing lacrimal fluid accumulation in the cavity.15–20 Few studies in the literature have examined the activity of the orbicularis oculi muscles after prosthesis installation,21 and all of them have been based solely on clinical observations. Thus, the purpose of this study was to determine whether the muscle tone is influenced by prosthesis installation. Accordingly, the electrical activities of the superior and inferior orbicularis muscles (SO and IO, respectively) were evaluated before and after ocular prostheses were installed in patients with unilateral enucleation of the ocular bulb. The study hypothesis was that rehabilitative treatment with an ocular prosthesis would affect the electrical activity of the orbicularis muscles. Patients and methods
Fig. 1. MyosystemBr1 electromyograph and bipolar surface electrodes.
was adjusted to 2000 times. To visualize and process the EMG signal, Myosystem I software version 2.12 was used. Bipolar surface electrodes (DataHominis Tecnologia Ltda) were used for EMG recording. Electrodes were positioned on the SO and IO muscles of both eyes (the enucleated eye and the healthy eye) (Fig. 2)20. The EMG signal was captured in four clinical situations: rest, normal opening and closing of the eyelids (OCE), rapid opening and closing of the eyelids (ROC), and squeezing. Each situation was recorded for 10 s. EMG examinations were performed before and 7, 14, 30, and 60 days after the ocular prosthesis was installed and in use. The EMG record of the orbicularis muscle of the patient’s healthy eye was used as the control.
Participant selection
The study included 12 volunteers (age range 50–65 years) with unilateral enucleation of the ocular globe (time since ocular globe loss 6–24 months) and an indication for a prosthesis, based on anamnesis and clinical examinations. Exclusion criteria were as follows: prior use of an ocular or expander prosthesis; extreme atresia of the anophthalmic cavity; and an inability to perform the tests due to insufficient cognitive ability. Volunteers received information about the treatment to be used and signed a consent form, in accordance with the recommendations of the institutional ethics committee for human research.
Manufacture of the ocular prosthesis
An ocular prosthesis was made individually for each patient, according to the technique described by Goiato et al.22 Data analysis
Two-way repeated-measures analysis of variance (ANOVA) was performed to verify whether there were statistically
Electromyographic examination
Electromyographic (EMG) examinations were performed with the MyosystemBr1 electromyograph (DataHominis Tecnologia Ltda, Uberlaˆndia, Minas Gerais, Brazil) (Fig. 1). EMG signals were conditioned using instrument amplifiers, which were programmable via software, and analogue band-pass filters with 10-Hz highband and 1000-Hz low-band frequencies. Signals were digitized with a sampling frequency of 2 kHz, with 12 bits of resolution and simultaneous signal sampling. For data collection, the equipment gain
Fig. 2. Bipolar surface electrodes positioned on the superior (SO) and inferior (IO) orbicularis oculi muscles of the eye.
significant differences between the muscles and periods (time points) for each clinical condition. The means were compared by Tukey–Kramer honestly significant difference (HSD) tests using SPSS version 19.0 statistical software (SPSS Inc., Chicago, IL, USA). All the results were analysed at a significance level of 0.05. Results
Table 1 shows the electrical activity values for each clinical condition (rest, OCE, ROC, and squeezing), muscle (location analysed, SO and IO), and time point (initial, 7, 14, 30, 60 days and control). ANOVA revealed a significant difference (P < 0.0001) in the electrical activity values for time point in all clinical conditions (Tables 2–5). There was significantly higher electrical activity according to the muscle in all clinical situations but squeezing (ANOVA, Table 5, muscle P > 0.05). In addition there was no significant difference in the interaction of all factors for the clinical conditions of rest, OCE, and squeezing (P > 0.05) (Tables 2, 3 and 5). However, there was a statistically significant difference in the interaction of all factors for the ROC condition (Table 4). The electrical activity levels of the ROC condition exhibited significantly higher values for the SO muscle than the IO muscle for each time period, excepting the baseline (Tables 1 and 4). The electrical activity levels at different times were significantly different from the initial (baseline) value under all four clinical conditions evaluated, regardless of the muscle (Table 6). Under the clinical conditions of rest, OCE, and ROC, the SO was significantly more active than the IO for all times (initial, 7, 14, 30, and 60 days and control) (Table 7). Under the clinical condition of squeezing, although the SO showed greater activity than the IO, the difference was not statistically significant (Table 7).
Electrical activity of the orbicularis muscles
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Table 1. Electromyographic activity (mV) of the orbicularis muscles for analysed clinical conditions at different times after installing the ocular prosthesis.a Condition
Period (days)
Muscle
Control
Baseline
7
14
30
60
Rest
SO IO
8.42 2.12 5.93 1.62
10.03 2.13 7.82 2.30
10.62 1.81 8.16 2.03
10.82 1.88 8.19 1.84
10.89 1.85 8.22 1.96
10.87 1.90 8.55 1.82
OCE
SO IO
9.27 1.93 7.89 2.02
12.18 2.15 10.39 2.15
12.69 1.94 10.77 1.99
12.89 1.88 10.83 1.98
12.89 1.98 10.94 2.04
12.62 1.53 10.94 1.48
ROC
SO IO
13.32 2.92 10.88 2.96
22.74 3.51 15.84 3.81
24.93 2.89 17.99 4.32
25.77 3.41 18.49 4.63
25.81 3.49 18.78 4.94
25.18 3.40 18.48 2.95
Squeezing
SO IO
76.68 17.02 65.85 19.01
118.97 14.93 108.80 15.38
127.78 22.44 113.96 21.17
130.05 23.01 116.66 20.82
131.50 21.05 117.12 19.41
135.51 24.25 124.73 23.50
SO, superior orbicularis; IO, inferior orbicularis; OCE, normal opening and closing of the eyes; ROC, rapid opening and closing of the eyes. a Data are shown as the mean standard deviation. The control was the contralateral healthy eye.
Table 2. Results of two-way repeated-measures ANOVA for the rest condition.
Discussion
Variation factors
df
SS
MS
F
P-value
Muscle Between subjects Period Period muscle Within subjects
1 22 5 5 110
218.415 458.275 108.909 0.903 42.174
218.415 20.831 21.782 0.181 0.383
10.485
0.004*
56.813 0.471
<0.0001* 0.797
ANOVA, analysis of variance. * P < 0.05 denotes a statistically significant difference.
Table 3. Results of two-way repeated-measures ANOVA for the OCE condition. Variation factors
df
SS
MS
F
P-value
Muscle Between subjects Period Period muscle Within subjects
1 22 5 5 110
116.268 429.028 201.858 1.788 64.009
116.268 19.501 40.372 0.358 0.582
5.962
0.023*
69.379 0.615
<0.0001* 0.689
ANOVA, analysis of variance; OCE, normal opening and closing of the eyes. * P < 0.05 denotes a statistically significant difference.
Table 4. Results of two-way repeated-measures ANOVA for the ROC condition. Variation factors
df
SS
MS
F
P-value
Muscle Between subjects Period Period muscle Within subjects
1 22 5 5 110
1390.741 1276.058 1874.628 103.563 494.677
1390.741 58.003 374.926 20.713 4.497
23.977
<0.0001*
83.371 4.606
<0.0001* 0.001*
ANOVA, analysis of variance; ROC, rapid opening and closing of the eyes. * P < 0.05 denotes a statistically significant difference.
Table 5. Results of two-way repeated-measures ANOVA for the squeezing condition. Variation factors
df
SS
MS
Muscle Between subjects Period Period muscle Within subjects
1 22 5 5 110
5382.506 43,931.345 55,852.655 100.888 10,907.938
5382.506 1996.879 11,170.531 20.178 99.163
ANOVA, analysis of variance. * P < 0.05 denotes a statistically significant difference.
F 2.695 112.648 0.203
P-value 0.115 <0.0001* 0.961
Rehabilitative treatment with an ocular prosthesis stimulated the EMG activity of the orbicularis muscles, restoring some muscle tone; therefore, the hypothesis of this study was accepted. The increase in electrical activity of the muscles occurred after the patient had used the prosthesis for only 1 week under all analysed clinical conditions (rest, OCE, ROC, and squeezing). Within 14 days after installing the prosthesis, the activities of the SO and IO muscles approached those of the contralateral eye, which acted as the control. These results offer evidence of a functional equilibrium between the sides, and the importance of using an ocular prosthesis to restore normal motor function to the person. Unfortunately, there are few studies broaching this subject in the available literature. Specifically, a search of the literature revealed only one relevant study, in which the authors compared the electrical activity of the orbicularis oculi muscle between normal individuals and those receiving ocular prostheses.21 Regalo et al. evaluated 24 men (mean age 32.5 years), including 12 normal subjects (control group) and 12 individuals with absence of the left eyeball who were scheduled to receive ocular prostheses. In the ocular prosthesis group, the absence of the eyeball was due to different aetiological factors, including trauma and infection (toxoplasmosis). Examination by EMG (K6-I EMG Light Channel Surface EMG; Myotronics, Seattle, WA, USA) was performed before and after prosthesis placement under four clinical conditions: initial rest, normal opening and closing of the eyelids, opening and forced closure of the eyelids, and final rest. Surface electrodes were positioned on the lateral portion of the orbicularis oculi muscle.
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Table 6. Electromyographic activity (mV) of the orbicularis muscles for each clinical condition of the study among different times, regardless of the muscle.a Condition Rest OCE ROC Squeezing
Period (days)
Control
Baseline
7
14
30
60
7.18 2.24 b 8.58 2.06 b 12.10 3.14 b 71.27 18.49 b
8.92 2.45 c 11.29 2.29 c 19.29 5.02 c 113.89 15.71 c
9.39 2.26 c 11.73 2.16 c 21.46 5.05 c 120.87 22.47c
9.51 2.26 c 11.86 2.16 c 22.13 5.44 c 123.36 22.53 c
9.55 2.31 c 11.91 2.20 c 22.30 5.51 c 124.31 21.12 c
9.71 2.17 c 11.78 1.70 c 21.83 4.63 c 130.12 23.99 c
OCE, normal opening and closing of the eyes; ROC, rapid opening and closing of the eyes. a Data are shown as the mean standard deviation.b,c Averages followed by different letters in lowercase in the line differ significantly (P < 0.05). Table 7. Electromyographic activity (mV) of the orbicularis muscles for each clinical condition of the study among muscles, regardless of the different times.a Condition
Muscle IO
SO Rest OCE ROC Squeezing
b
10.27 2.08 12.09 2.25 b 22.96 5.47 b 120.08 28.41 b
7.81 2.06 c 10.29 2.18 c 16.74 4.78 c 107.85 27.45 b
SO, superior orbicularis; IO, inferior orbicularis. a Data are shown as the mean standard deviation.b,c Averages followed by different letters in lowercase in the line differ significantly (P < 0.05).
Regalo et al. reported that prosthesis use did not interfere with the clinical conditions of opening and closing the eyelid. Loss of the eyeball increased the EMG activity of the orbicularis oculi muscle, and prosthesis use for 7 days (i.e., during prosthesis adaptation) was insufficient to decrease muscle activity. However, the authors cannot directly compare their results to those of Regalo et al. because of differences in patient selection, methods, and aspects of data analysis. The increase in electrical activity found in our study may stem from an increase in muscle force. When the muscle is inactive for long periods of time, the contractile proteins degrade and the number of myofibrils decreases, leading to cellular atrophy.6 Installing an ocular prosthesis might increase myofibril production, leading to better orbicularis oculi muscle tone. The increase in electrical activity may also be related to the type of prosthesis that was built. The prosthesis was made individually for each patient, by moulding the anophthalmic cavity. This procedure ensures intimate contact between the prosthesis and the tissues, facilitating the correct adaptation of the prosthesis to the cavity and to the muscles, and conferring mobility to the prosthesis. As a result, the patient moves his or her muscles more, resulting in an increase in electrical activity. During the clinical condition of rest, EMG activity was observed during all of the periods analysed. This result is in agreement with the study by Patel and
Shahani,23 who observed that during electrical activity, there was no rest position (or relaxation of the extraocular muscles) and the muscles were always active. However, a lower level of electrical activity for the muscles was anticipated during rest compared to the other clinical conditions. In rest, any change in facial equilibrium, such as the installation of an ocular prosthesis, can cause changes to muscle tension, a finding verified by this study. The orbicularis oculi muscle performs the mechanism of sphincter or dilatory movement, controlling the degree to which the eyelids open and shut.6–8 In the clinical condition of OCE, the main function of this muscle is to protect the eyes. The authors verified that using an ocular prosthesis promoted functional stimulation in the OCE condition within 7 and 14 days – an equilibrium that was maintained over the time course analysed (60 days), with similar values to the patient’s healthy eye (the contralateral control). The above result was also observed during the ROC condition (i.e. blinking). In addition to serving as an important protective factor, blinking distributes tears across the cornea, maintaining a smooth surface and promoting foreign body removal.6 The EMG values obtained in the initial analysis of the ROC condition were lower than values for the other periods analysed. This result is perhaps because the patient, before rehabilitation, was unable to blink safely. From the moment that the ocular prosthesis was installed, it
provided the necessary support for the person to blink, allowing the patient to do this movement safely. The results most approached the values for the healthy eye (the control) after the ocular prosthesis had been used for 30 days. Because blinking requires control and precision, the patient may have needed more time to relearn how to make this movement. Under the clinical condition of squeezing, the authors observed a statistically significant increase in the values for the electrical activity of the orbicularis oculi muscle over time. Clinically, this result is very important, as it provides evidence that the lack of an ocular bulb can promote changes in the activation pattern of the peri-orbital musculature, making it hypofunctional. Soon after installation of the ocular prosthesis (7–14 days), the organism re-established itself, and the fibres returned to a form of action similar to that of the normal eye. Values for electrical activity during squeezing were much higher than those for the other clinical conditions. This finding may be related to the fact that the orbicularis oculi muscle is an important sphincter muscle. Its fibres are spread in concentric circles around the orbital margin and in the eyelids, integrating with the cutaneous muscle group of the head, which is responsible for facial movements and expression.6–8,24 The muscle is positioned around the eye, greatly exceeding the limits of the orbit.6–8,24 The act of forcefully closing the eyelid is executed in collaboration with the orbital part, moving the front, temporal, and cheek skin in the direction of the average angle of the eyelids.6–8,24 Thus, during squeezing, the authors believe that the orbicularis oculi muscle was helped by the facial muscles, leading to a much higher electrical activity. With respect to the superior and inferior fasciculi of the orbicularis oculi muscle, the authors verified that the upper lid had more activity than the lower lid in all clinical conditions, with statistically significant values for the conditions of rest, OCE, and ROC. This finding may also be
Electrical activity of the orbicularis muscles related to the presence of other muscles in the upper part, such as the levator palpebrae superioris, which is normally preserved in the anophthalmic cavity after enucleation of the ocular bulb,9–13 aiding the movement of the future prosthesis. Most patients reported more tearing in the ocular globe after prosthesis installation. This observation is of great importance to this study. Various authors have affirmed that the objective of an ocular prosthesis is to re-establish the facial aesthetics while maintaining the cavity’s anatomical form, inhibiting eyelid collapse, directing tear drainage, preventing fluid accumulation in the cavity, maintaining muscle tone, and protecting the cavity.1– 3,5,15–22 Therefore, a prosthesis should be installed in a manner such that the tear ducts—which previously might have been obstructed because of muscle atresia—are reactivated. Another important clinical finding was the time needed for the patient to adapt to the ocular prosthesis (7–14 days). After this time, the values of electrical activity for all of the clinical conditions analysed remained constant. Importantly, the results of this study might have been different if the volunteers had not been rehabilitated within 24 months of ocular bulb loss. In our opinion, the longer the interval between enucleation and prosthesis installation, the harder it is for the patient to adapt to the prosthesis, due to atresia of the eyelids and hypofunction of the muscles. The greatest difficulty in executing this study came from the positioning of the electrodes on the muscles. This step required a technically proficient and careful operator to position them adequately, such that the superior and inferior parts of the muscle were analysed, and not the lateral part. To clarify the behaviour of the ocular prosthesis relative to the peri-orbital musculature, future longitudinal studies should be performed. Such studies should also evaluate other factors, such as the presence or absence of orbital implants and the different techniques used to obtain the prosthesis. In conclusion, rehabilitative treatment with ocular prostheses for patients with unilateral anophthalmia promotes an increase in the electrical activity of orbicularis oculi muscles, re-establishing some of the muscle tone and motor function to the muscles in the area affected by the defect. Funding
Supported by grant from State of Sa˜o Paulo Research Foundation (FAPESP) and PIBIC/CNPq.
Competing interests
None. Ethical approval
This study was approved by the Faculty of Dentistry of Arac¸atuba, UNESP – Universidade Estadual Paulista (Process FOA 01053/2011). Patient consent
Volunteers signed a consent form, in accordance with the recommendations of the Ethics Committee for Human Research of the Universidade Estadual Paulista. References ´ ., 1. Goulart DR, Queiroz E, Fernandes A.U Oliveira LM. Psychosocial aspects in the rehabilitation of patients with anophthalmic socket: implications of the use of ocular prosthesis. Arq Bras Oftalmol 2011;74: 330–4. 2. Goiato MC, dos Santos DM, Bannwart LC, Moreno A, Pesqueira AA, Haddad MF, et al. Psychosocial impact on anophthalmic patients wearing ocular prosthesis. Int J Oral Maxillofac Surg 2013;42:113–9. 3. Song JS, Oh J, Baek SH. A survey of satisfaction in anophthalmic patients wearing ocular prosthesis. Graefes Arch Clin Exp Ophthalmol 2006;244:330–5. 4. Coˆas VR, Neves AC, Rode SdeM. Evaluation of the etiology of ocular globe atrophy or loss. Braz Dent J 2005;16:243–6. 5. Jayaswal GP, Dange SP, Khalikar AN. Restoration of an atrophic eye socket with custom made eye prosthesis, utilizing digital photography. Indian J Dent Res 2011;22: 482–5. 6. Kakizaki H, Malhotra R, Selva D. Upper eyelid anatomy: an update. Ann Plast Surg 2009;63:336–43. 7. Plock J, Contaldo C, von Lu¨dinghausen M. Levator palpebrae superioris muscle in human fetuses: anatomical findings and their clinical relevance. Clin Anat 2005;18: 473–80. 8. Porter JD, Burns LA, May PJ. Morphological substrate for eyelid movements: innervation and structure of primate levator palpebrae superioris and orbicularis oculi muscles. J Comp Neurol 1989;287:64–81. [9] Sophie Yi JY, Dierks EJ, Over LM, Hauck MJ. Prosthetic reconstruction of the orbit/ globe. Oral Maxillofac Surg Clin North Am 2012;24:697–712. 10. Soares IP, Franc¸a VP. Evisceration and enucleation. Semin Ophthalmol 2010;25:94–7. 11. Goiato MC, Demathe´ A, Suzuki T, dos Santos DM, Dekon SF. Management of orbital reconstruction. J Craniofac Surg 2010;21: 1834–6.
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12. Markiewicz MR, Bell RB. Traditional and contemporary surgical approaches to the orbit. Oral Maxillofac Surg Clin North Am 2012;24:573–607. 13. Zheng C, Wu AY. Enucleation versus evisceration in ocular trauma: a retrospective review and study of current literature. Orbit 2013;32:356–61. 14. Nassab RS, Thomas SS, Murray D. Orbital exenteration for advanced periorbital skin cancers: 20 years experience. J Plast Reconstr Aesthet Surg 2007;60:1103–9. 15. Shrivastava S, Agarwal S, Shrivastava KJ, Tyagi P. Custom-made ocular prosthesis for a pediatric patient with unilateral anophthalmia: a case report. J Indian Soc Pedod Prev Dent 2013;31:194–6. 16. Hatamleh MM, Haylock C, Hollows P, Richmond A, Watson J. Prosthetic eye rehabilitation and management of completely blind patients. Int J Prosthodont 2012;25:631–5. 17. Garg P, Garg S, Bansal D, Suresh S. Prosthetic rehabilitation of a patient with enucleated eye – a case report. Nepal J Ophthalmol 2012;4:312–4. 18. Raizada K, Rani D. Ocular prosthesis. Cont Lens Anterior Eye 2007;30:152. 19. Goiato MC, Mancuso DN, Sundefeld ML, Gabriel MB, Murakawa AC, Guiotti AM. Aesthetic and functional ocular rehabilitation. Oral Oncology Extra 2005;41:162–4. 20. Willis J, Weyland S, McRobbie I. Orbital anatomy for rehabilitation: the ocularist’s point of view. Adv Ophthal Plast Reconstr Surg 1990;8:58–68. 21. Regalo SC, Vitti M, Semprini M, Tosello DdeO, Lopes RA, de Matos MdaG, et al. EMG activity of the orbicularis oculi muscle in normal and in individuals indicated to receive eye prosthesis, before and after its placement. Electromyogr Clin Neurophysiol 2002;42:17–23. 22. Goiato MC, dos Santos DM, Moreno A, Filie´ Haddad M, Turcio KH. An alternate impression technique for ocular prostheses. J Prosthodont 2013;22:338–40. 23. Patel RC, Shahani M. Electromyography of extraocular muscles (EOM). Indian J Ophthalmol 1973;21:2–4. 24. Vigliante CE. Anatomy and functions of the muscles of facial expression. Oral Maxillofac Surg Clin North Am 2005;17:1–15.
Address: Marcelo Coelho Goiato Department of Dental Materials and Prosthodontics Arac¸atuba Dental School Sa˜o Paulo State University Jose´ Bonifa´cio 1193 Arac¸atuba Sa˜o Paulo 16015-050 Brazil. Fax: +55 18 3636 3245 E-mail: [email protected]
Clinical Paper Clinical Pathology
Electrical activity of the orbicularis muscles before and after installation of ocular prostheses
M. C. Goiato, M. R. Santos, B. C. Z. Monteiro, A. Moreno, L. C. Bannwart, A. J. V. Filho, A. M. Guiotti, M. F. Haddad, A. A. Pesqueira, D. M. dos Santos Oral Oncology Centre, School of Dentistry of Arac¸atuba, UNESP, Universidade Estadual Paulista, Arac¸atuba, Sa˜o Paulo, Brazil
M. C. Goiato, M. R. Santos, B. C. Z. Monteiro, A. Moreno, L. C. Bannwart, A. J. V. Filho, A. M. Guiotti, M. F. Haddad, A. A. Pesqueira, D. M. dos Santos: Electrical activity of the orbicularis muscles before and after installation of ocular prostheses. Int. J. Oral Maxillofac. Surg. 2015; 44: 127–131. # 2014 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Abstract. This study examined the electrical activity of the superior (SO) and inferior (IO) orbicularis oculi muscles before and after installing ocular prostheses in patients who had undergone unilateral enucleation. Twelve volunteers requiring prostheses were selected. Their electrical activity was monitored at rest and during normal opening and closing of the eyelids, rapid opening and closing of the eyelids, and squeezing. Data were recorded before and 7, 30, and 60 days after the ocular prosthesis was installed. Two-way analysis of variance was performed to verify whether there were any significant differences between the muscles and periods, and means were compared by Tukey–Kramer honestly significant difference (HSD) tests (P < 0.05). Results from the initial period differed significantly from those after prosthesis installation in all clinical situations. The SO had significantly higher electrical activity levels than the IO in all clinical situations but squeezing. The authors observed the same values during the initial period for the condition of rest (SO 8.42/IO 5.93) and the highest values for the condition of squeezing after 60 days (SO 131.50/IO 117.12). Rehabilitative treatment promoted an increase in the electrical activity of the orbicularis oculi muscles, restoring part of the muscle tone and motor function to muscles of the affected area.
Orbital defects are embarrassing to patients because they affect the face, which is essential to human relationships.1–3 The absence of an ocular globe can lead to atrophy of the orbicularis muscles of the eye, thereby altering the muscle tone of the facial area.4,5 The 0901-5027/010127 + 05
palpebral cutaneous musculature is of supreme importance to facial appearance and expression, and it protects the ocular cavities.6–8 Three ocular–orbital–palpebral surgeries are related to ocular bulb removal: evisceration, comprising the partial removal of the ocular bulb with
Key words: eye enucleation; eye; artificial; electromyography. Accepted for publication 19 September 2014 Available online 3 November 2014
conservation of the sclera; enucleation, comprising the total removal of the bulb with only the capsule and oculomotor muscles remaining; and exenteration, comprising the removal of all contents of the orbital cavity and the circumjacent tissue.9–14
# 2014 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
128
Goiato et al.
To rehabilitate patients with deformities of the ocular bulb, an ocular prosthesis may be used.15–20 Prosthesis use improves the patient’s aesthetic appearance, helping their psychosocial development and improving their quality of life.1–3 The prosthesis does not restore the original function of vision, but it keeps the anophthalmic cavity filled, restoring lacrimal direction and preventing lacrimal fluid accumulation in the cavity.15–20 Few studies in the literature have examined the activity of the orbicularis oculi muscles after prosthesis installation,21 and all of them have been based solely on clinical observations. Thus, the purpose of this study was to determine whether the muscle tone is influenced by prosthesis installation. Accordingly, the electrical activities of the superior and inferior orbicularis muscles (SO and IO, respectively) were evaluated before and after ocular prostheses were installed in patients with unilateral enucleation of the ocular bulb. The study hypothesis was that rehabilitative treatment with an ocular prosthesis would affect the electrical activity of the orbicularis muscles. Patients and methods
Fig. 1. MyosystemBr1 electromyograph and bipolar surface electrodes.
was adjusted to 2000 times. To visualize and process the EMG signal, Myosystem I software version 2.12 was used. Bipolar surface electrodes (DataHominis Tecnologia Ltda) were used for EMG recording. Electrodes were positioned on the SO and IO muscles of both eyes (the enucleated eye and the healthy eye) (Fig. 2)20. The EMG signal was captured in four clinical situations: rest, normal opening and closing of the eyelids (OCE), rapid opening and closing of the eyelids (ROC), and squeezing. Each situation was recorded for 10 s. EMG examinations were performed before and 7, 14, 30, and 60 days after the ocular prosthesis was installed and in use. The EMG record of the orbicularis muscle of the patient’s healthy eye was used as the control.
Participant selection
The study included 12 volunteers (age range 50–65 years) with unilateral enucleation of the ocular globe (time since ocular globe loss 6–24 months) and an indication for a prosthesis, based on anamnesis and clinical examinations. Exclusion criteria were as follows: prior use of an ocular or expander prosthesis; extreme atresia of the anophthalmic cavity; and an inability to perform the tests due to insufficient cognitive ability. Volunteers received information about the treatment to be used and signed a consent form, in accordance with the recommendations of the institutional ethics committee for human research.
Manufacture of the ocular prosthesis
An ocular prosthesis was made individually for each patient, according to the technique described by Goiato et al.22 Data analysis
Two-way repeated-measures analysis of variance (ANOVA) was performed to verify whether there were statistically
Electromyographic examination
Electromyographic (EMG) examinations were performed with the MyosystemBr1 electromyograph (DataHominis Tecnologia Ltda, Uberlaˆndia, Minas Gerais, Brazil) (Fig. 1). EMG signals were conditioned using instrument amplifiers, which were programmable via software, and analogue band-pass filters with 10-Hz highband and 1000-Hz low-band frequencies. Signals were digitized with a sampling frequency of 2 kHz, with 12 bits of resolution and simultaneous signal sampling. For data collection, the equipment gain
Fig. 2. Bipolar surface electrodes positioned on the superior (SO) and inferior (IO) orbicularis oculi muscles of the eye.
significant differences between the muscles and periods (time points) for each clinical condition. The means were compared by Tukey–Kramer honestly significant difference (HSD) tests using SPSS version 19.0 statistical software (SPSS Inc., Chicago, IL, USA). All the results were analysed at a significance level of 0.05. Results
Table 1 shows the electrical activity values for each clinical condition (rest, OCE, ROC, and squeezing), muscle (location analysed, SO and IO), and time point (initial, 7, 14, 30, 60 days and control). ANOVA revealed a significant difference (P < 0.0001) in the electrical activity values for time point in all clinical conditions (Tables 2–5). There was significantly higher electrical activity according to the muscle in all clinical situations but squeezing (ANOVA, Table 5, muscle P > 0.05). In addition there was no significant difference in the interaction of all factors for the clinical conditions of rest, OCE, and squeezing (P > 0.05) (Tables 2, 3 and 5). However, there was a statistically significant difference in the interaction of all factors for the ROC condition (Table 4). The electrical activity levels of the ROC condition exhibited significantly higher values for the SO muscle than the IO muscle for each time period, excepting the baseline (Tables 1 and 4). The electrical activity levels at different times were significantly different from the initial (baseline) value under all four clinical conditions evaluated, regardless of the muscle (Table 6). Under the clinical conditions of rest, OCE, and ROC, the SO was significantly more active than the IO for all times (initial, 7, 14, 30, and 60 days and control) (Table 7). Under the clinical condition of squeezing, although the SO showed greater activity than the IO, the difference was not statistically significant (Table 7).
Electrical activity of the orbicularis muscles
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Table 1. Electromyographic activity (mV) of the orbicularis muscles for analysed clinical conditions at different times after installing the ocular prosthesis.a Condition
Period (days)
Muscle
Control
Baseline
7
14
30
60
Rest
SO IO
8.42 2.12 5.93 1.62
10.03 2.13 7.82 2.30
10.62 1.81 8.16 2.03
10.82 1.88 8.19 1.84
10.89 1.85 8.22 1.96
10.87 1.90 8.55 1.82
OCE
SO IO
9.27 1.93 7.89 2.02
12.18 2.15 10.39 2.15
12.69 1.94 10.77 1.99
12.89 1.88 10.83 1.98
12.89 1.98 10.94 2.04
12.62 1.53 10.94 1.48
ROC
SO IO
13.32 2.92 10.88 2.96
22.74 3.51 15.84 3.81
24.93 2.89 17.99 4.32
25.77 3.41 18.49 4.63
25.81 3.49 18.78 4.94
25.18 3.40 18.48 2.95
Squeezing
SO IO
76.68 17.02 65.85 19.01
118.97 14.93 108.80 15.38
127.78 22.44 113.96 21.17
130.05 23.01 116.66 20.82
131.50 21.05 117.12 19.41
135.51 24.25 124.73 23.50
SO, superior orbicularis; IO, inferior orbicularis; OCE, normal opening and closing of the eyes; ROC, rapid opening and closing of the eyes. a Data are shown as the mean standard deviation. The control was the contralateral healthy eye.
Table 2. Results of two-way repeated-measures ANOVA for the rest condition.
Discussion
Variation factors
df
SS
MS
F
P-value
Muscle Between subjects Period Period muscle Within subjects
1 22 5 5 110
218.415 458.275 108.909 0.903 42.174
218.415 20.831 21.782 0.181 0.383
10.485
0.004*
56.813 0.471
<0.0001* 0.797
ANOVA, analysis of variance. * P < 0.05 denotes a statistically significant difference.
Table 3. Results of two-way repeated-measures ANOVA for the OCE condition. Variation factors
df
SS
MS
F
P-value
Muscle Between subjects Period Period muscle Within subjects
1 22 5 5 110
116.268 429.028 201.858 1.788 64.009
116.268 19.501 40.372 0.358 0.582
5.962
0.023*
69.379 0.615
<0.0001* 0.689
ANOVA, analysis of variance; OCE, normal opening and closing of the eyes. * P < 0.05 denotes a statistically significant difference.
Table 4. Results of two-way repeated-measures ANOVA for the ROC condition. Variation factors
df
SS
MS
F
P-value
Muscle Between subjects Period Period muscle Within subjects
1 22 5 5 110
1390.741 1276.058 1874.628 103.563 494.677
1390.741 58.003 374.926 20.713 4.497
23.977
<0.0001*
83.371 4.606
<0.0001* 0.001*
ANOVA, analysis of variance; ROC, rapid opening and closing of the eyes. * P < 0.05 denotes a statistically significant difference.
Table 5. Results of two-way repeated-measures ANOVA for the squeezing condition. Variation factors
df
SS
MS
Muscle Between subjects Period Period muscle Within subjects
1 22 5 5 110
5382.506 43,931.345 55,852.655 100.888 10,907.938
5382.506 1996.879 11,170.531 20.178 99.163
ANOVA, analysis of variance. * P < 0.05 denotes a statistically significant difference.
F 2.695 112.648 0.203
P-value 0.115 <0.0001* 0.961
Rehabilitative treatment with an ocular prosthesis stimulated the EMG activity of the orbicularis muscles, restoring some muscle tone; therefore, the hypothesis of this study was accepted. The increase in electrical activity of the muscles occurred after the patient had used the prosthesis for only 1 week under all analysed clinical conditions (rest, OCE, ROC, and squeezing). Within 14 days after installing the prosthesis, the activities of the SO and IO muscles approached those of the contralateral eye, which acted as the control. These results offer evidence of a functional equilibrium between the sides, and the importance of using an ocular prosthesis to restore normal motor function to the person. Unfortunately, there are few studies broaching this subject in the available literature. Specifically, a search of the literature revealed only one relevant study, in which the authors compared the electrical activity of the orbicularis oculi muscle between normal individuals and those receiving ocular prostheses.21 Regalo et al. evaluated 24 men (mean age 32.5 years), including 12 normal subjects (control group) and 12 individuals with absence of the left eyeball who were scheduled to receive ocular prostheses. In the ocular prosthesis group, the absence of the eyeball was due to different aetiological factors, including trauma and infection (toxoplasmosis). Examination by EMG (K6-I EMG Light Channel Surface EMG; Myotronics, Seattle, WA, USA) was performed before and after prosthesis placement under four clinical conditions: initial rest, normal opening and closing of the eyelids, opening and forced closure of the eyelids, and final rest. Surface electrodes were positioned on the lateral portion of the orbicularis oculi muscle.
130
Goiato et al.
Table 6. Electromyographic activity (mV) of the orbicularis muscles for each clinical condition of the study among different times, regardless of the muscle.a Condition Rest OCE ROC Squeezing
Period (days)
Control
Baseline
7
14
30
60
7.18 2.24 b 8.58 2.06 b 12.10 3.14 b 71.27 18.49 b
8.92 2.45 c 11.29 2.29 c 19.29 5.02 c 113.89 15.71 c
9.39 2.26 c 11.73 2.16 c 21.46 5.05 c 120.87 22.47c
9.51 2.26 c 11.86 2.16 c 22.13 5.44 c 123.36 22.53 c
9.55 2.31 c 11.91 2.20 c 22.30 5.51 c 124.31 21.12 c
9.71 2.17 c 11.78 1.70 c 21.83 4.63 c 130.12 23.99 c
OCE, normal opening and closing of the eyes; ROC, rapid opening and closing of the eyes. a Data are shown as the mean standard deviation.b,c Averages followed by different letters in lowercase in the line differ significantly (P < 0.05). Table 7. Electromyographic activity (mV) of the orbicularis muscles for each clinical condition of the study among muscles, regardless of the different times.a Condition
Muscle IO
SO Rest OCE ROC Squeezing
b
10.27 2.08 12.09 2.25 b 22.96 5.47 b 120.08 28.41 b
7.81 2.06 c 10.29 2.18 c 16.74 4.78 c 107.85 27.45 b
SO, superior orbicularis; IO, inferior orbicularis. a Data are shown as the mean standard deviation.b,c Averages followed by different letters in lowercase in the line differ significantly (P < 0.05).
Regalo et al. reported that prosthesis use did not interfere with the clinical conditions of opening and closing the eyelid. Loss of the eyeball increased the EMG activity of the orbicularis oculi muscle, and prosthesis use for 7 days (i.e., during prosthesis adaptation) was insufficient to decrease muscle activity. However, the authors cannot directly compare their results to those of Regalo et al. because of differences in patient selection, methods, and aspects of data analysis. The increase in electrical activity found in our study may stem from an increase in muscle force. When the muscle is inactive for long periods of time, the contractile proteins degrade and the number of myofibrils decreases, leading to cellular atrophy.6 Installing an ocular prosthesis might increase myofibril production, leading to better orbicularis oculi muscle tone. The increase in electrical activity may also be related to the type of prosthesis that was built. The prosthesis was made individually for each patient, by moulding the anophthalmic cavity. This procedure ensures intimate contact between the prosthesis and the tissues, facilitating the correct adaptation of the prosthesis to the cavity and to the muscles, and conferring mobility to the prosthesis. As a result, the patient moves his or her muscles more, resulting in an increase in electrical activity. During the clinical condition of rest, EMG activity was observed during all of the periods analysed. This result is in agreement with the study by Patel and
Shahani,23 who observed that during electrical activity, there was no rest position (or relaxation of the extraocular muscles) and the muscles were always active. However, a lower level of electrical activity for the muscles was anticipated during rest compared to the other clinical conditions. In rest, any change in facial equilibrium, such as the installation of an ocular prosthesis, can cause changes to muscle tension, a finding verified by this study. The orbicularis oculi muscle performs the mechanism of sphincter or dilatory movement, controlling the degree to which the eyelids open and shut.6–8 In the clinical condition of OCE, the main function of this muscle is to protect the eyes. The authors verified that using an ocular prosthesis promoted functional stimulation in the OCE condition within 7 and 14 days – an equilibrium that was maintained over the time course analysed (60 days), with similar values to the patient’s healthy eye (the contralateral control). The above result was also observed during the ROC condition (i.e. blinking). In addition to serving as an important protective factor, blinking distributes tears across the cornea, maintaining a smooth surface and promoting foreign body removal.6 The EMG values obtained in the initial analysis of the ROC condition were lower than values for the other periods analysed. This result is perhaps because the patient, before rehabilitation, was unable to blink safely. From the moment that the ocular prosthesis was installed, it
provided the necessary support for the person to blink, allowing the patient to do this movement safely. The results most approached the values for the healthy eye (the control) after the ocular prosthesis had been used for 30 days. Because blinking requires control and precision, the patient may have needed more time to relearn how to make this movement. Under the clinical condition of squeezing, the authors observed a statistically significant increase in the values for the electrical activity of the orbicularis oculi muscle over time. Clinically, this result is very important, as it provides evidence that the lack of an ocular bulb can promote changes in the activation pattern of the peri-orbital musculature, making it hypofunctional. Soon after installation of the ocular prosthesis (7–14 days), the organism re-established itself, and the fibres returned to a form of action similar to that of the normal eye. Values for electrical activity during squeezing were much higher than those for the other clinical conditions. This finding may be related to the fact that the orbicularis oculi muscle is an important sphincter muscle. Its fibres are spread in concentric circles around the orbital margin and in the eyelids, integrating with the cutaneous muscle group of the head, which is responsible for facial movements and expression.6–8,24 The muscle is positioned around the eye, greatly exceeding the limits of the orbit.6–8,24 The act of forcefully closing the eyelid is executed in collaboration with the orbital part, moving the front, temporal, and cheek skin in the direction of the average angle of the eyelids.6–8,24 Thus, during squeezing, the authors believe that the orbicularis oculi muscle was helped by the facial muscles, leading to a much higher electrical activity. With respect to the superior and inferior fasciculi of the orbicularis oculi muscle, the authors verified that the upper lid had more activity than the lower lid in all clinical conditions, with statistically significant values for the conditions of rest, OCE, and ROC. This finding may also be
Electrical activity of the orbicularis muscles related to the presence of other muscles in the upper part, such as the levator palpebrae superioris, which is normally preserved in the anophthalmic cavity after enucleation of the ocular bulb,9–13 aiding the movement of the future prosthesis. Most patients reported more tearing in the ocular globe after prosthesis installation. This observation is of great importance to this study. Various authors have affirmed that the objective of an ocular prosthesis is to re-establish the facial aesthetics while maintaining the cavity’s anatomical form, inhibiting eyelid collapse, directing tear drainage, preventing fluid accumulation in the cavity, maintaining muscle tone, and protecting the cavity.1– 3,5,15–22 Therefore, a prosthesis should be installed in a manner such that the tear ducts—which previously might have been obstructed because of muscle atresia—are reactivated. Another important clinical finding was the time needed for the patient to adapt to the ocular prosthesis (7–14 days). After this time, the values of electrical activity for all of the clinical conditions analysed remained constant. Importantly, the results of this study might have been different if the volunteers had not been rehabilitated within 24 months of ocular bulb loss. In our opinion, the longer the interval between enucleation and prosthesis installation, the harder it is for the patient to adapt to the prosthesis, due to atresia of the eyelids and hypofunction of the muscles. The greatest difficulty in executing this study came from the positioning of the electrodes on the muscles. This step required a technically proficient and careful operator to position them adequately, such that the superior and inferior parts of the muscle were analysed, and not the lateral part. To clarify the behaviour of the ocular prosthesis relative to the peri-orbital musculature, future longitudinal studies should be performed. Such studies should also evaluate other factors, such as the presence or absence of orbital implants and the different techniques used to obtain the prosthesis. In conclusion, rehabilitative treatment with ocular prostheses for patients with unilateral anophthalmia promotes an increase in the electrical activity of orbicularis oculi muscles, re-establishing some of the muscle tone and motor function to the muscles in the area affected by the defect. Funding
Supported by grant from State of Sa˜o Paulo Research Foundation (FAPESP) and PIBIC/CNPq.
Competing interests
None. Ethical approval
This study was approved by the Faculty of Dentistry of Arac¸atuba, UNESP – Universidade Estadual Paulista (Process FOA 01053/2011). Patient consent
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Address: Marcelo Coelho Goiato Department of Dental Materials and Prosthodontics Arac¸atuba Dental School Sa˜o Paulo State University Jose´ Bonifa´cio 1193 Arac¸atuba Sa˜o Paulo 16015-050 Brazil. Fax: +55 18 3636 3245 E-mail: [email protected]