Anatomy & Physiology
Regional Variations in Orbicularis Oculi Histology Bryan R. Costin, M.D.*, Thomas P. Plesec, M.D.†, Laura J. Kopplin, M.D., Ph.D.‡, Rao V. Chundury, M.D., M.B.A.*, Jennifer M. McBride, Ph.D.§, Mark R. Levine, M.D.║, and Julian D. Perry, M.D.* *Cole Eye Institute, Cleveland Clinic, Cleveland, Ohio and †Department of Anatomic Pathology, Cleveland Clinic, Cleveland, Ohio; ‡Casey Eye Institute, Oregon Health and Science University, Portland, Oregon; §Department of Anatomy, Cleveland Clinic Lerner College of Medicine, Cleveland, Ohio; ║Lorain Institute, Cleveland Clinic, Lorain, Ohio.
Purpose: To investigate and compare the histologic compositions of the pretarsal, preseptal, and orbital orbicularis oculi muscle (OOM) using nonpreserved, fresh-frozen, human cadavers. Methods: The OOM was exposed using sharp and blunt dissection. A metric ruler was used to measure and mark 0.5 cm × 1 cm samples from each portion of the right, superior OOM. Samples were excised, fixed in formalin, and completely embedded in paraffin. Five-micrometer-thick, hematoxylinand eosin-stained sections were generated for each sample and analyzed by an anatomical pathologist. The relative percentages of the 4 main tissue types (skeletal muscle, fibrous tissue, adipose tissue, and neurovascular tissue) were quantified. Results: Forty-two samples were obtained from 14 Caucasian cadavers. On average, the pretarsal samples were composed of 83.5% skeletal muscle, 0.0% adipose, 5.0% neurovascular, and 11.5% fibrous tissue. Average preseptal OOM was 46.5% skeletal muscle, 12.7% adipose, 9.2% neurovascular, and 31.5% fibrous tissue. The orbital OOM was, on average, 42.7% skeletal muscle, 32.7% adipose tissue, 6.9% neurovascular, and 17.7% fibrous tissue. Conclusions: The OOM represents a histologically heterogeneous structure. (Ophthal Plast Reconstr Surg 2015;31:325–327)
T
he orbicularis oculi (orbicularis palpebrarum) muscle is critical to ocular health and an essential structure in ophthalmic plastic surgery and neurotoxin therapy. The protractor is composed of pretarsal and preseptal portions (collectively, the pars palpebralis) and an orbital portion (pars orbitalis).1,2 In general, the former controls involuntary narrowing of the palpebral fissure and the latter produces eyelid closure with increasing force and volition. The orbital orbicularis also acts as a major eyebrow depressor.3,4 Along the eyelid margin, a very small component of the orbicularis called the muscle of Riolan likely plays a role in meibomian gland secretion, eyelid-globe apposition, and cilia position.2,5,6 A PubMed search in September 2014 using the search parameter “orbicularis oculi” yielded 1,522 titles with only a few studies on orbicularis microstructure. Most of these studies explored microscopic relationships to other structures, specific muscle fiber types, or stained for neuromuscular junction Accepted for publication January 14, 2015. The authors have no financial or conflicts of interest to disclose. Address correspondence and reprint requests to Bryan R. Costin, M.D., Cole Eye Institute, Cleveland Clinic, 9500 Euclid Ave., Cleveland, OH 44195. E-mail: [email protected] DOI: 10.1097/IOP.0000000000000430
Ophthal Plast Reconstr Surg, Vol. 31, No. 4, 2015
locations.7–15 Despite its importance, the authors are not aware of previous comparative histologic studies. They sought to compare the histologic compositions of the pretarsal, preseptal, and orbital orbicularis using light microscopic examination of freshfrozen cadaveric human tissue.
METHODS This study was performed using nonpreserved human cadavers registered in the Cleveland Clinic Body Donation Program. Specimens were excluded from this study if previous head and/or neck dissection had been performed or if there were signs of ocular and periocular trauma including cornea donation. The same surgeon (B.R.C.) performed all dissections and all measurements. Only the right upper eyelid was dissected, and this location was chosen at random. Data collection included age, gender, and race. Superficial skin incisions were created 1 cm lateral and parallel to a line connecting the supraorbital notch and the infraorbital foramen and from the lateral canthus to the superior border of the tragus. The orbicularis oculi muscle (OOM) was exposed using a combination of sharp and blunt dissection and 1.0 cm horizontal × 0.5 cm vertical rectangles were excised using a no. 15 blade, 0.5 mm forceps, and Westcott scissors (Fig. 1). Each specimen was fixed in 10% buffered formalin, completely embedded in paraffin, cut in a singe 5-μm-thick section, and stained with hematoxylin and eosin. Each sample was evaluated by light microscopy at ×2 magnification for relative quantities of the 4 main histologic components, including skeletal muscle, fibrous tissue, adipose tissue, and neurovascular tissue by an anatomical pathologist (T.P.P.; Figs. 2–4). Percentages were determined by visual inspection and estimation using a technique similar to that described by Markin et al.16 for hepatic adiposity. Continuous
FIG. 1. External photograph of cadaver no. 10 demonstrates the dissected orbicularis with 0.5 cm × 1.0 cm sections marked for excision and analysis.
325
Copyright © 2015 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc. Unauthorized reproduction of this article is prohibited.
Ophthal Plast Reconstr Surg, Vol. 31, No. 4, 2015
B. R. Costin et al.
measures were summarized using means and standard deviations, and statistical analysis was performed using SAS Software (version 9.1; Cary, NC).
RESULTS
FIG. 2. Low-power (×2 magnification) photomicrograph of hematoxylin- and eosin-stained pretarsal orbicularis sample from specimen no. 13 showing predominantly skeletal muscle and neurovascular tissue (NV).
A total of 42 samples were obtained from 14 fresh-frozen human cadavers. All specimens were obtained from the right, superior OOM, and all cadavers were Caucasian. Nine were male. Average age at time of death was 73.0 ± 15.9 years (range 35–93 years). On average, the pretarsal orbicularis was composed of 83.5% ± 10.1% skeletal muscle, 0.0% ± 0.0% adipose, 5.0% ± 0.0% neurovascular, and 11.5% ± 10.1% fibrous tissue. The average preseptal OOM was 46.5% ± 22.0% skeletal muscle, 12.7% ± 13.2% adipose, 9.2% ± 11.0% neurovascular, and 31.5% ± 17.4% fibrous tissue. The orbital OOM was, on average, 42.7% ± 17.6% skeletal muscle, 32.7% ± 16.9% adipose tissue, 6.9% ± 2.5% neurovascular, and 17.7% ± 8.6% fibrous tissue (Table).
DISCUSSION
FIG. 3. Low-power (×2 magnification) photomicrograph of hematoxylin- and eosin-stained preseptal orbicularis sample from specimen no. 13 showing predominantly skeletal muscle interspersed with neurovascular (NV), fibrous (F), and adipose (A) tissue (×2 magnification).
FIG. 4. Low-power (×2 magnification) photomicrograph of hematoxylin- and eosin-stained orbital orbicularis sample from specimen no. 13 showing predominantly skeletal muscle interspersed with adipose (A), fibrous (F), and neurovascular (NV) tissue.
Despite its importance, surprisingly few studies have explored the compositions of the OOM. The microstructure of the OOM does seem quite heterogeneous (Table). The differences in the tissue at the microscopic level may imply divergent functions as the biologic adage, “structure dictates function,” would suggest. The higher percentage (31.5%) of fibrous tissue within the preseptal OOM suggests that the orbital septum may invest in the OOM. Exploring the relationship of this fibrous tissue to the septum at the arcus marginalis may provide insight. Perhaps the preseptal OOM possesses fibrous tissue independent of the septum for the purposes of scaffolding. Interestingly, the preseptal region represents a relatively unsupported portion of the OOM, which, unlike the pretarsal and orbital portions, lacks denser deep tissue support (i.e., the tarsal plate and the orbital rim, respectively). A lattice of fibrous tissue throughout the preseptal OOM continuous with the orbital septum could represent a mechanism of deep support to this region. The high adiposity (32.7%) of the orbital orbicularis may speak to this portion’s metabolic demands or its proximity to the eyebrow fat pad or both. Borodic17 suggested a “glide” function imparted by adipose tissue overlying and underlying the orbicularis: “the suborbicularis orbital fat pad provides a lowresistance ‘slippery’ surface, allowing a high-amplitude brow and denser soft tissue movement concentrically inward.” Indeed, it appears from the data in this study that fatty tissues not only sandwich the OOM but also account for a third of the muscle’s substance histologically, perhaps lowering friction to facilitate eyebrow and eyelid movements. Size may factor into the tissue differences in this study. The pretarsal orbicularis is much smaller than the preseptal OOM and even smaller than the orbital portion. Therefore, it may not be surprising that the pretarsal OOM is nearly all skeletal muscle compared with the other portions. It is interesting that despite the size differences and tissue heterogeneity, the neurovascular tissue was relatively conserved among the 3 portions of the OOM. This finding may imply that, per surface area, there are more neurons innervating the muscle fibers of the pretarsal OOM than the preseptal and orbital portions. Implications
Percentage skeletal muscle, adipose, neurovascular, and fibrous tissue Pretarsal Preseptal Orbital
326
Skeletal muscle
Adipose
Neurovascular
Fibrous
83.5% ± 10.1% 46.5% ± 22.0% 42.7% ± 17.6%
0.0% ± 0.0% 12.7% ± 13.2% 32.7% ± 16.9%
5.0% ± 0.0% 9.2% ± 11.0% 6.9% ± 2.5%
11.5% ± 10.1% 31.5% ± 17.4% 17.7% ± 8.6%
© 2015 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc.
Copyright © 2015 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc. Unauthorized reproduction of this article is prohibited.
Ophthal Plast Reconstr Surg, Vol. 31, No. 4, 2015
for neurotoxin administration are clear, and it has been shown that low doses to the pretarsal OOM are safe and effective.18 Limitations of this study include the use of cadaveric specimens and the use of only right upper eyelid tissue. However, the use of nonpreserved specimens removes the possible effects of tissue preservatives and the opportunity to obtain uniform samples of all 3 portions of the OOM from the same specimen rarely presents itself in vivo. Advanced age may account for some of the findings, but Pottier et al.19 showed that orbicularis changes little with age and most involution occurs in the cutaneous and subcutaneous palpebral tissues.20,21 Sampling error may have incorporated other tissues (e.g., subcutaneous tissue, orbital septum, retro-orbicularis fat). However, 5-μm-thick samples make it more likely that OOM was analyzed rather than fragments of neighboring tissues. Finally, tissue types were estimated by a single observer using visual inspection of the specimens under light microscopy. Further study using digital software to confirm the authors’ findings would be valuable. To the authors’ knowledge, no previous studies have evaluated or compared the 3 portions of the OOM histologically. The microstructural differences found in this compact yet important anatomical area likely relate to the different functions of each of the 3 zones. The structure-function relationship of the OOM is often envisioned as the pars palpebralis mediating involuntary blink while the preseptal and to a greater extent the orbital OOM control the more forceful volitional blink. However, the individual zones of the OOM, and the OOM as a whole, likely function in a more complex way. If a structure as small as the muscle of Riolan can act in meibomian secretion, cilia position, and eyelid apposition, then the much larger portions of the OOM may have more functions that are currently recognized.5 Further investigation in the microstructure of the OOM may clarify functional contributions of each zone and demonstrate senescent changes that can be improved with rejuvenative techniques.
REFERENCES 1. Whitnall SE. The Anatomy of the Human Orbit and Accessory Organs of Vision. London: Henry Frowde and Hodder & Stoughton, 1921:125–30. 2. American Academy of Ophthalmology: Basic and Clinical Science Course. Section 7: Orbit, Eyelids, and Lacrimal System; San Fransisco: Americal Academy of Ophthalmology; 2011–2012; 136. 3. Drake RL, Vogl W, Mitchell AWM, et al. Gray’s Atlas of Anatomy. Philadelphia, PA: Elsevier, 2007:808.
Orbicularis Oculi Histology
4. Costin BR, Plesec TP, Sakolsatayadorn N, et al. Anatomy and histology of the frontalis muscle. Ophthal Plast Reconstr Surg 2015;31:66–72. 5. Lipham WJ, Tawfik HA, Dutton JJ. A histologic analysis and threedimensional reconstruction of the muscle of Riolan. Ophthal Plast Reconstr Surg 2002;18:93–8. 6. Lemke BN, Lucarelli MJ. Anatomy of the ocular adnexa, orbit, and related facial structures. In: Black EH, Nesi FA, Calvano CJ, eds. Smith and Nesi’s Ophthalmic Plastic and Reconstructive Surgery. 3rd ed. New York: Springer, 2012:22–3. 7. Klodt J. Zur vergleichenden anatomie der lid-muskululatur. Arch für Mikos Anat 1893;41:1–18. 8. Kuwabara T, Cogan DG, Johnson CC. Structure of the muscles of the upper eyelid. Arch Ophthalmol 1975;93:1189–97. 9. Nelson CC, Blaivas M. Orbicularis oculi muscle in children. Histologic and histochemical characteristics. Invest Ophthalmol Vis Sci 1991;32:646–54. 10. Borodic GE, Cozzolino D, Ferrante R, et al. Innervation zone of orbicularis oculi muscle and implications for botulinum A toxin therapy. Ophthal Plast Reconstr Surg 1991;7:54–60. 11. McLoon LK, Wirtschafter JD. Regional differences in the orbicularis oculi muscle: conservation between species. J Neurol Sci 1991;104:197–202. 12. Manners RM, Weller RO. Histochemical staining of orbicularis oculi muscle in ectropion and entropion. Eye (Lond) 1994;8 (pt 3):332–5. 13. Wirtschafter JD, Lander T, Baker RH, et al. Heterogeneous length and in-series arrangement of orbicularis oculi muscle: individual myofibers do not extend the length of the eyelid. Trans Am Ophthalmol Soc 1994;92:71–88. 14. Cheng NC, Liao SL, Wang IJ, et al. Fiber type and myosin heavy chain compositions of adult pretarsal orbicularis oculi muscle. J Mol Histol 2007;38:177–82. 15. Hwang K, Huan F, Kim DJ. Muscle fiber types of human orbicularis oculi muscle. J Craniofac Surg 2011;22:1827–30. 16. Markin RS, Wisecarver JL, Radio SJ, et al. Frozen section evaluation of donor livers before transplantation. Transplantation 1993;56:1403–9. 17. Borodic GE. Functional significance of fat surrounding the orbicularis oculi muscle. Ophthal Plast Reconstr Surg 2010;26:501–2. 18. Huang L, Costin BR, Sakolsatayadorn N, et al. Safety of onabotulinum toxin a injection to the central upper eyelid and eyebrow regions. Ophthal Plast Reconstr Surg 2014;30:377–80. 19. Pottier F, El-Shazly NZ, El-Shazly AE. Aging of orbicularis oculi: anatomophysiologic consideration in upper blepharoplasty. Arch Facial Plast Surg 2008;10:346–9. 20. Goldberg RA. Orbicularis muscle aging. JAMA Ophthalmol 2013;131:94. 21. Lee H, Park M, Lee J, et al. Histopathologic findings of the orbicularis oculi in upper eyelid aging: total or minimal excision of orbicularis oculi in upper blepharoplasty. Arch Facial Plast Surg 2012;14:253–7.
© 2015 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc.
327
Copyright © 2015 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc. Unauthorized reproduction of this article is prohibited.
Regional Variations in Orbicularis Oculi Histology Bryan R. Costin, M.D.*, Thomas P. Plesec, M.D.†, Laura J. Kopplin, M.D., Ph.D.‡, Rao V. Chundury, M.D., M.B.A.*, Jennifer M. McBride, Ph.D.§, Mark R. Levine, M.D.║, and Julian D. Perry, M.D.* *Cole Eye Institute, Cleveland Clinic, Cleveland, Ohio and †Department of Anatomic Pathology, Cleveland Clinic, Cleveland, Ohio; ‡Casey Eye Institute, Oregon Health and Science University, Portland, Oregon; §Department of Anatomy, Cleveland Clinic Lerner College of Medicine, Cleveland, Ohio; ║Lorain Institute, Cleveland Clinic, Lorain, Ohio.
Purpose: To investigate and compare the histologic compositions of the pretarsal, preseptal, and orbital orbicularis oculi muscle (OOM) using nonpreserved, fresh-frozen, human cadavers. Methods: The OOM was exposed using sharp and blunt dissection. A metric ruler was used to measure and mark 0.5 cm × 1 cm samples from each portion of the right, superior OOM. Samples were excised, fixed in formalin, and completely embedded in paraffin. Five-micrometer-thick, hematoxylinand eosin-stained sections were generated for each sample and analyzed by an anatomical pathologist. The relative percentages of the 4 main tissue types (skeletal muscle, fibrous tissue, adipose tissue, and neurovascular tissue) were quantified. Results: Forty-two samples were obtained from 14 Caucasian cadavers. On average, the pretarsal samples were composed of 83.5% skeletal muscle, 0.0% adipose, 5.0% neurovascular, and 11.5% fibrous tissue. Average preseptal OOM was 46.5% skeletal muscle, 12.7% adipose, 9.2% neurovascular, and 31.5% fibrous tissue. The orbital OOM was, on average, 42.7% skeletal muscle, 32.7% adipose tissue, 6.9% neurovascular, and 17.7% fibrous tissue. Conclusions: The OOM represents a histologically heterogeneous structure. (Ophthal Plast Reconstr Surg 2015;31:325–327)
T
he orbicularis oculi (orbicularis palpebrarum) muscle is critical to ocular health and an essential structure in ophthalmic plastic surgery and neurotoxin therapy. The protractor is composed of pretarsal and preseptal portions (collectively, the pars palpebralis) and an orbital portion (pars orbitalis).1,2 In general, the former controls involuntary narrowing of the palpebral fissure and the latter produces eyelid closure with increasing force and volition. The orbital orbicularis also acts as a major eyebrow depressor.3,4 Along the eyelid margin, a very small component of the orbicularis called the muscle of Riolan likely plays a role in meibomian gland secretion, eyelid-globe apposition, and cilia position.2,5,6 A PubMed search in September 2014 using the search parameter “orbicularis oculi” yielded 1,522 titles with only a few studies on orbicularis microstructure. Most of these studies explored microscopic relationships to other structures, specific muscle fiber types, or stained for neuromuscular junction Accepted for publication January 14, 2015. The authors have no financial or conflicts of interest to disclose. Address correspondence and reprint requests to Bryan R. Costin, M.D., Cole Eye Institute, Cleveland Clinic, 9500 Euclid Ave., Cleveland, OH 44195. E-mail: [email protected] DOI: 10.1097/IOP.0000000000000430
Ophthal Plast Reconstr Surg, Vol. 31, No. 4, 2015
locations.7–15 Despite its importance, the authors are not aware of previous comparative histologic studies. They sought to compare the histologic compositions of the pretarsal, preseptal, and orbital orbicularis using light microscopic examination of freshfrozen cadaveric human tissue.
METHODS This study was performed using nonpreserved human cadavers registered in the Cleveland Clinic Body Donation Program. Specimens were excluded from this study if previous head and/or neck dissection had been performed or if there were signs of ocular and periocular trauma including cornea donation. The same surgeon (B.R.C.) performed all dissections and all measurements. Only the right upper eyelid was dissected, and this location was chosen at random. Data collection included age, gender, and race. Superficial skin incisions were created 1 cm lateral and parallel to a line connecting the supraorbital notch and the infraorbital foramen and from the lateral canthus to the superior border of the tragus. The orbicularis oculi muscle (OOM) was exposed using a combination of sharp and blunt dissection and 1.0 cm horizontal × 0.5 cm vertical rectangles were excised using a no. 15 blade, 0.5 mm forceps, and Westcott scissors (Fig. 1). Each specimen was fixed in 10% buffered formalin, completely embedded in paraffin, cut in a singe 5-μm-thick section, and stained with hematoxylin and eosin. Each sample was evaluated by light microscopy at ×2 magnification for relative quantities of the 4 main histologic components, including skeletal muscle, fibrous tissue, adipose tissue, and neurovascular tissue by an anatomical pathologist (T.P.P.; Figs. 2–4). Percentages were determined by visual inspection and estimation using a technique similar to that described by Markin et al.16 for hepatic adiposity. Continuous
FIG. 1. External photograph of cadaver no. 10 demonstrates the dissected orbicularis with 0.5 cm × 1.0 cm sections marked for excision and analysis.
325
Copyright © 2015 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc. Unauthorized reproduction of this article is prohibited.
Ophthal Plast Reconstr Surg, Vol. 31, No. 4, 2015
B. R. Costin et al.
measures were summarized using means and standard deviations, and statistical analysis was performed using SAS Software (version 9.1; Cary, NC).
RESULTS
FIG. 2. Low-power (×2 magnification) photomicrograph of hematoxylin- and eosin-stained pretarsal orbicularis sample from specimen no. 13 showing predominantly skeletal muscle and neurovascular tissue (NV).
A total of 42 samples were obtained from 14 fresh-frozen human cadavers. All specimens were obtained from the right, superior OOM, and all cadavers were Caucasian. Nine were male. Average age at time of death was 73.0 ± 15.9 years (range 35–93 years). On average, the pretarsal orbicularis was composed of 83.5% ± 10.1% skeletal muscle, 0.0% ± 0.0% adipose, 5.0% ± 0.0% neurovascular, and 11.5% ± 10.1% fibrous tissue. The average preseptal OOM was 46.5% ± 22.0% skeletal muscle, 12.7% ± 13.2% adipose, 9.2% ± 11.0% neurovascular, and 31.5% ± 17.4% fibrous tissue. The orbital OOM was, on average, 42.7% ± 17.6% skeletal muscle, 32.7% ± 16.9% adipose tissue, 6.9% ± 2.5% neurovascular, and 17.7% ± 8.6% fibrous tissue (Table).
DISCUSSION
FIG. 3. Low-power (×2 magnification) photomicrograph of hematoxylin- and eosin-stained preseptal orbicularis sample from specimen no. 13 showing predominantly skeletal muscle interspersed with neurovascular (NV), fibrous (F), and adipose (A) tissue (×2 magnification).
FIG. 4. Low-power (×2 magnification) photomicrograph of hematoxylin- and eosin-stained orbital orbicularis sample from specimen no. 13 showing predominantly skeletal muscle interspersed with adipose (A), fibrous (F), and neurovascular (NV) tissue.
Despite its importance, surprisingly few studies have explored the compositions of the OOM. The microstructure of the OOM does seem quite heterogeneous (Table). The differences in the tissue at the microscopic level may imply divergent functions as the biologic adage, “structure dictates function,” would suggest. The higher percentage (31.5%) of fibrous tissue within the preseptal OOM suggests that the orbital septum may invest in the OOM. Exploring the relationship of this fibrous tissue to the septum at the arcus marginalis may provide insight. Perhaps the preseptal OOM possesses fibrous tissue independent of the septum for the purposes of scaffolding. Interestingly, the preseptal region represents a relatively unsupported portion of the OOM, which, unlike the pretarsal and orbital portions, lacks denser deep tissue support (i.e., the tarsal plate and the orbital rim, respectively). A lattice of fibrous tissue throughout the preseptal OOM continuous with the orbital septum could represent a mechanism of deep support to this region. The high adiposity (32.7%) of the orbital orbicularis may speak to this portion’s metabolic demands or its proximity to the eyebrow fat pad or both. Borodic17 suggested a “glide” function imparted by adipose tissue overlying and underlying the orbicularis: “the suborbicularis orbital fat pad provides a lowresistance ‘slippery’ surface, allowing a high-amplitude brow and denser soft tissue movement concentrically inward.” Indeed, it appears from the data in this study that fatty tissues not only sandwich the OOM but also account for a third of the muscle’s substance histologically, perhaps lowering friction to facilitate eyebrow and eyelid movements. Size may factor into the tissue differences in this study. The pretarsal orbicularis is much smaller than the preseptal OOM and even smaller than the orbital portion. Therefore, it may not be surprising that the pretarsal OOM is nearly all skeletal muscle compared with the other portions. It is interesting that despite the size differences and tissue heterogeneity, the neurovascular tissue was relatively conserved among the 3 portions of the OOM. This finding may imply that, per surface area, there are more neurons innervating the muscle fibers of the pretarsal OOM than the preseptal and orbital portions. Implications
Percentage skeletal muscle, adipose, neurovascular, and fibrous tissue Pretarsal Preseptal Orbital
326
Skeletal muscle
Adipose
Neurovascular
Fibrous
83.5% ± 10.1% 46.5% ± 22.0% 42.7% ± 17.6%
0.0% ± 0.0% 12.7% ± 13.2% 32.7% ± 16.9%
5.0% ± 0.0% 9.2% ± 11.0% 6.9% ± 2.5%
11.5% ± 10.1% 31.5% ± 17.4% 17.7% ± 8.6%
© 2015 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc.
Copyright © 2015 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc. Unauthorized reproduction of this article is prohibited.
Ophthal Plast Reconstr Surg, Vol. 31, No. 4, 2015
for neurotoxin administration are clear, and it has been shown that low doses to the pretarsal OOM are safe and effective.18 Limitations of this study include the use of cadaveric specimens and the use of only right upper eyelid tissue. However, the use of nonpreserved specimens removes the possible effects of tissue preservatives and the opportunity to obtain uniform samples of all 3 portions of the OOM from the same specimen rarely presents itself in vivo. Advanced age may account for some of the findings, but Pottier et al.19 showed that orbicularis changes little with age and most involution occurs in the cutaneous and subcutaneous palpebral tissues.20,21 Sampling error may have incorporated other tissues (e.g., subcutaneous tissue, orbital septum, retro-orbicularis fat). However, 5-μm-thick samples make it more likely that OOM was analyzed rather than fragments of neighboring tissues. Finally, tissue types were estimated by a single observer using visual inspection of the specimens under light microscopy. Further study using digital software to confirm the authors’ findings would be valuable. To the authors’ knowledge, no previous studies have evaluated or compared the 3 portions of the OOM histologically. The microstructural differences found in this compact yet important anatomical area likely relate to the different functions of each of the 3 zones. The structure-function relationship of the OOM is often envisioned as the pars palpebralis mediating involuntary blink while the preseptal and to a greater extent the orbital OOM control the more forceful volitional blink. However, the individual zones of the OOM, and the OOM as a whole, likely function in a more complex way. If a structure as small as the muscle of Riolan can act in meibomian secretion, cilia position, and eyelid apposition, then the much larger portions of the OOM may have more functions that are currently recognized.5 Further investigation in the microstructure of the OOM may clarify functional contributions of each zone and demonstrate senescent changes that can be improved with rejuvenative techniques.
REFERENCES 1. Whitnall SE. The Anatomy of the Human Orbit and Accessory Organs of Vision. London: Henry Frowde and Hodder & Stoughton, 1921:125–30. 2. American Academy of Ophthalmology: Basic and Clinical Science Course. Section 7: Orbit, Eyelids, and Lacrimal System; San Fransisco: Americal Academy of Ophthalmology; 2011–2012; 136. 3. Drake RL, Vogl W, Mitchell AWM, et al. Gray’s Atlas of Anatomy. Philadelphia, PA: Elsevier, 2007:808.
Orbicularis Oculi Histology
4. Costin BR, Plesec TP, Sakolsatayadorn N, et al. Anatomy and histology of the frontalis muscle. Ophthal Plast Reconstr Surg 2015;31:66–72. 5. Lipham WJ, Tawfik HA, Dutton JJ. A histologic analysis and threedimensional reconstruction of the muscle of Riolan. Ophthal Plast Reconstr Surg 2002;18:93–8. 6. Lemke BN, Lucarelli MJ. Anatomy of the ocular adnexa, orbit, and related facial structures. In: Black EH, Nesi FA, Calvano CJ, eds. Smith and Nesi’s Ophthalmic Plastic and Reconstructive Surgery. 3rd ed. New York: Springer, 2012:22–3. 7. Klodt J. Zur vergleichenden anatomie der lid-muskululatur. Arch für Mikos Anat 1893;41:1–18. 8. Kuwabara T, Cogan DG, Johnson CC. Structure of the muscles of the upper eyelid. Arch Ophthalmol 1975;93:1189–97. 9. Nelson CC, Blaivas M. Orbicularis oculi muscle in children. Histologic and histochemical characteristics. Invest Ophthalmol Vis Sci 1991;32:646–54. 10. Borodic GE, Cozzolino D, Ferrante R, et al. Innervation zone of orbicularis oculi muscle and implications for botulinum A toxin therapy. Ophthal Plast Reconstr Surg 1991;7:54–60. 11. McLoon LK, Wirtschafter JD. Regional differences in the orbicularis oculi muscle: conservation between species. J Neurol Sci 1991;104:197–202. 12. Manners RM, Weller RO. Histochemical staining of orbicularis oculi muscle in ectropion and entropion. Eye (Lond) 1994;8 (pt 3):332–5. 13. Wirtschafter JD, Lander T, Baker RH, et al. Heterogeneous length and in-series arrangement of orbicularis oculi muscle: individual myofibers do not extend the length of the eyelid. Trans Am Ophthalmol Soc 1994;92:71–88. 14. Cheng NC, Liao SL, Wang IJ, et al. Fiber type and myosin heavy chain compositions of adult pretarsal orbicularis oculi muscle. J Mol Histol 2007;38:177–82. 15. Hwang K, Huan F, Kim DJ. Muscle fiber types of human orbicularis oculi muscle. J Craniofac Surg 2011;22:1827–30. 16. Markin RS, Wisecarver JL, Radio SJ, et al. Frozen section evaluation of donor livers before transplantation. Transplantation 1993;56:1403–9. 17. Borodic GE. Functional significance of fat surrounding the orbicularis oculi muscle. Ophthal Plast Reconstr Surg 2010;26:501–2. 18. Huang L, Costin BR, Sakolsatayadorn N, et al. Safety of onabotulinum toxin a injection to the central upper eyelid and eyebrow regions. Ophthal Plast Reconstr Surg 2014;30:377–80. 19. Pottier F, El-Shazly NZ, El-Shazly AE. Aging of orbicularis oculi: anatomophysiologic consideration in upper blepharoplasty. Arch Facial Plast Surg 2008;10:346–9. 20. Goldberg RA. Orbicularis muscle aging. JAMA Ophthalmol 2013;131:94. 21. Lee H, Park M, Lee J, et al. Histopathologic findings of the orbicularis oculi in upper eyelid aging: total or minimal excision of orbicularis oculi in upper blepharoplasty. Arch Facial Plast Surg 2012;14:253–7.
© 2015 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc.
327
Copyright © 2015 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc. Unauthorized reproduction of this article is prohibited.
