ANATOMICAL STUDY

Origin of the Lower Orbicularis Oculi Muscle in Relation to the Nasojugal Groove Kun Hwang, MD, PhD, Han Joon Kim, MD, MS, Hun Kim, BHS, Dae Joong Kim, PhD,y and Se Won Hwangz§ Abstract: The aim of this study was to clarify the location of the origin of the lower orbicularis oculi muscle (OOM) in relation to the nasojugal groove. In 45 lower eyelids of 44 patients, the origin of the lower OOM was identified. In 4 lower eyelids of 2 fresh cadavers, the breaking strength was measured. In 4 lower eyelids of 4 fixed cadavers, 3 parasagittal sections and 2 horizontal sections were made. In computed tomographic scans of 182 orbits of 99 patients, the maxillary attachment of the OOM was measured. The lower OOM originated along the orbital margin, and the mean (SD) width of the attachment was 10.5 (1.4) mm. The lower OOM ran obliquely laterally and downward. The force needed to tear the 3-mm–wide OOM was 8.40 (0.21) N. Histologically, the OOM was attached to the periosteum on the medial limbus line; however, it was not attached at the midpupillary line or the lateral limbus line. The most medial part of the lower OOM was attached to the periosteum. In the middle and lateral part of the lower eyelid, however, a fibrofatty tissue was found between the OOM and the periosteum. In computed tomographic scans, the OOM was almost always attached to the maxilla at the medial epicanthus (100%) and at the medial limbus line (92.3%). At the midpupillary line, fewer than half (45.6%) were attached. At the lateral limbus line (14.3%) and the lateral canthus (4.4%), they were rarely attached. In a relaxed state, the nasojugal groove is not evident because the attached portion does not pull at the wings. While squinting, the OOM contracts and the vertical width shortens, and thereafter, a surface puckering of the delicate periorbital skin appears. Key Words: Facial muscles, maxilla, anatomy and histology, tomography, x-ray computed (J Craniofac Surg 2015;26: 1389–1393)

From the Department of Plastic Surgery; yDepartment of Anatomy, Inha University School of Medicine, Incheon, Republic of Korea; zPeninsula Medical School, Exeter, UK; and §Inha Research Institute for Medical Science, Incheon, Republic of Korea. Received September 10, 2014. Accepted for publication January 22, 2015. Address correspondence and reprint requests to Dr. Kun Hwang, Department of Plastic Surgery, Inha University School of Medicine, 27 Inhang-ro, Jung-gu, Incheon, 400-711, Republic of Korea; E-mail: [email protected]; and Dae Joong Kim, PhD, Department of Anatomy, Inha University School of Medicine, 27 Inhang-ro, Jung-gu, Incheon, 400-711, Republic of Korea; E-mail: [email protected] Supported by a grant from Inha University (INHA-Research Grant). The authors report no conflict of interest. Copyright # 2015 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000001617

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ray’s Anatomy describes the orbital part of the orbicularis oculi muscle (OOM) arising from the nasal component of the frontal bone, the frontal process of the maxilla, and the medial palpebral ligament. Inferiorly and medially, the ellipses overlap or blend to some extent with adjacent muscles (levator labii superioris alaeque nasi, levator labii superioris, and zygomaticus minor).1 Recently, Haddock et al2 stated that the OOM is attached directly to the bone along the tear trough. The origin of the OOM was several millimeters (4–6 mm) below the orbital rim and the arcus marginalis in their cross-sectional illustration and description. On the contrary, Ghavami et al3 observed the origin of the OOM at the infraorbital rim and 2 to 3 mm above the supraorbital rim. The aim of this study was to clarify the exact location of the origin of the lower OOM in relation to the nasojugal groove.

MATERIALS AND METHODS Patients and Operative Measurements In 45 lower eyelids of 44 patients (39 men, 5 women) who underwent a subciliary approach, the origin of the lower OOM was identified (Fig. 1). The distances were measured using Marchac calipers. Among the 35 eyelids, 15 were left and 20 were right. The mean (SD) age of the patients was 41.0 (17.3) years. Measured distances: 1. Width of the palpebral fissure 2. Width of the attachment of the lower OOM along the orbital margin 3. Distance from the orbital margin at a midpoint distance from the palpebral fissure to the lower OOM 4. Distance from the arcus marginalis to the lower OOM at a midpoint distance of the palpebral fissure

Tension Measurement in Cadavers In 4 lower eyelids of 2 fresh cadavers (age 46 and 66 y, 2 men), the origin of the lower OOM was identified. A No. 5 silk thread (surgical suture nonabsorbable 100% silk; Bakje Co, Republic of Korea) was passed through the OOM at 6 mm lateral to the medial palpebral ligament, 3 mm apart, wound, and a 3-cm loop was made, which was pulled away using a tensiometer (BFG 20 N; Mesmecin Co, Sinfold, United Kingdom). The breaking strength was measured (Fig. 2).

Histology In 4 lower eyelids of 4 fixed cadavers (age range, 40–67 y, 4 men), the lower eyelid and the upper cheek were removed from the underlying bone fixed in a 10% neutral buffered formalin and embedded in paraffin. Three parasagittal sections were made at the medial limbus (ML) line, the midpupillary (MP) line, and the lateral limbus (LL) line. Two horizontal sections were made 8 mm below the ciliary margin and 16 mm below the ciliary margin (Fig. 3).

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FIGURE 1. The origin of the lower OOM is seen in a subciliary approach. F indicates orbital fat; L, LC; M, MC; O, OOM.



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FIGURE 4. Measured distance in the parasagittal view. AS indicates distance from the uppermost attachment of the lower OOM to the lowermost attachment; FM, distance from the arcus marginalis to the uppermost attachment of the lower OOM.

RESULTS Operative Measurement

FIGURE 2. Tension measurement of the OOM at its origin.

Ten-millimeter sections were stained with Masson-trichrome and then observed under a light microscope.

Measurement of Attachment of the OOM to the Maxilla In 182 orbits of 99 patients (70 men; age, 34.15 [16.72] y, and 29 women; age, 44.38 [21.05] y), the attachment of the OOM to the maxilla was measured. The patients underwent a three-dimensional facial computed tomographic scan from June 2013 to May 2014. Scans that were suggestive of facial trauma, edema, or swelling were excluded. In the parasagittal scans at 5 points (medial canthus [MC], ML, MP, LL, and lateral canthus [LC]), 2 distances were measured (Fig. 4):

The lower OOM originated along the orbital margin, and the mean (SD) width of the attachment was 10.5 (1.4) mm. The lower OOM ran obliquely laterally and downward. The distance from the orbital margin at a midpoint distance of the palpebral fissure to the lower OOM was 4.1 (1.5) mm. The distance from the arcus marginalis to the lower OOM at a midpoint distance of the palpebral fissure was 2.8 (0.9) mm. The half width of the palpebral fissure was 14.6 (1.1) mm. The angle between the axis origin of the OOM and the vertical line was 73.7 (4.7) degrees (Fig. 5).

Tension Measurement The force needed to tear the 3-mm–wide OOM 6 mm lateral to the medial canthal ligament was 8.40 (0.21) N.

Histology In parasagittal sections, the OOM was attached to the periosteum on the ML line; however, it was not attached at the MP line or at the

1. Free margin (FM): distance from the arcus marginalis to the uppermost attachment of the lower OOM 2. Attached span (AS): distance from the uppermost attachment of the lower OOM to the lowermost attachment

FIGURE 3. Schema of location and width of the origin of the lower OOM. L indicates LL line; M, ML line; P, MP line.

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FIGURE 5. Schema of OOM origin in an operative measurement. Unit: millimeters.

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Origin of Lower Orbicularis Oculi Muscle

TABLE 1. Average Length of Each Part of the OOM

AS FM

MC

ML

MP

LL

LC

P

5.35  2.03 0.77  0.90

3.90  2.37 1.00  1.07

1.87  2.38 0.60  1.06

0.56  1.51 0.12  0.53

0.11  0.53 0.10  0.60

.000 .000

MC, medial canthus; ML, medial limbus; MP, mid pupillary line; LL, lateral limbus; LC, lateral canthus; AS, attached span; FM, free margin.

TABLE 2. Statistical Difference of the Attached Span (AS, White Cells) and the Free Margin (FM, Gray Cells) FIGURE 6. Parasagittal sections through the ML line (left), the MP line (middle), and the LL line (right). Left, The origin of the OOM was attached to the periosteum approximately 2 mm inferior to the arcus marginalis (arrowhead). Middle, A fibrofatty tissue of 2- to 3-mm thickness was found between the OOM and the periosteum. The nearest point of the OOM to the periosteum was approximately 3 mm inferior to the arcus marginalis. Right, A fibrofatty tissue of 4- to 5-mm thickness was found between the OOM and the periosteum. The nearest point of the OOM to the periosteum was approximately 4 mm inferior to the arcus marginalis. Bar ¼ 4 mm. L indicates levator labii superioris muscle; O, OOM.

FIGURE 7. Horizontal sections 8 mm below (top) and 16 mm below (bottom) the ciliary margin. Top, The most medial part of the lower OOM was attached to the periosteum (dotted line). In the middle and lateral parts of the lower eyelid, the OOM was not attached to the periosteum and a fibrofatty tissue was found between the OOM and the periosteum. Bottom, No attachment of the OOM to the periosteum was observed. A fibrofatty tissue was found between the OOM and the periosteum throughout its course. Bar ¼ 2 mm. AN indicates levator labii superioris alique nasi; O, OOM.

LL line. On the ML line, the origin of the OOM was attached to the periosteum approximately 2 mm inferior to the arcus marginalis (arrowhead). On the MP line, a fibrofatty tissue 2 to 3 mm in thickness was found between the OOM and the periosteum. The nearest point of the OOM to the periosteum was approximately 3 mm inferior to the arcus marginalis. On the LL line, a fibrofatty

AS FM MC ML MP LL LC 

 0.000  0.000  0.000

LL

LC

 0.000  0.000

 0.000  0.000  0.000

 0.000  0.000  0.000 1.000

 0.000  0.000

0.276

FIGURE 9. Schema of attachment of the OOM (shaded area) on the orbital rim.

tissue 4 to 5 mm in thickness was found between the OOM and the periosteum. The nearest point of the OOM to the periosteum was approximately 4 mm inferior to the arcus marginalis (Fig. 6). In horizontal sections at 8 mm below the ciliary margin, the most medial part of the lower OOM was attached to the periosteum (dotted line). In the middle and lateral parts of the lower eyelid, TABLE 3. Average Length and Statistical Difference of Each Part of the OOM According to Gender

MC

LL LC Total

2015 Mutaz B. Habal, MD



MP

Statistically different; ANOVA (Scheffe).

MP

#

ML 0.000

0.154 0.445  0.000  0.000

ML

FIGURE 8. Frequency of attachment of the OOM to the maxilla (in 182 sides).

MC

AS FM AS FM AS FM AS FM AS FM AS FM

Total (182)

Male (126)

5.35  2.03 0.77  0.90 3.90  2.37 1.00  1.07 1.87  2.38 0.60  1.06 0.56  1.51 0.12  0.53 0.11  0.53 0.10  0.60 2.36  2.75 0.52  0.93

5.87  1.98 0.61  0.79 4.35  2.43 0.87  1.03 2.25  2.53 0.66  1.13 0.71  1.71 0.16  0.62 0.14  0.61 0.13  0.69 2.66  2.93 0.48  0.92

> < > < > 6 > > > 6 > 6

Female (56)

P

4.20  1.65 1.13  1.01 2.87  1.87 1.31  1.10 1.02  1.74 0.46  0.89 0.22  0.85 0.03  0.17 0.03  0.23 0.04  0.33 1.67  2.14 0.60  0.95

.000 .001 .000 .013 .000 .221 .010 .039 .075 .248 .000 .095

MC, medial canthus; ML, medial limbus; MP, mid pupillary line; LL, lateral limbus; LC, lateral canthus; AS, attached span; FM, free margin; , larger than right in statistically; 6, no statistical difference.

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TABLE 4. Average Length and Statistical Difference of Each Part of the OOM According to the Location

MC ML MP LL LC Total

AS FM AS FM AS FM AS FM AS FM AS FM

Total (182)

Left (90)

5.35  2.03 0.77  0.90 3.90  2.37 1.00  1.07 1.87  2.38 0.60  1.06 0.56  1.51 0.12  0.53 0.11  0.53 0.10  0.60 2.36  2.75 0.52  0.93

5.50  2.17 0.67  0.80 3.87  2.45 0.90  0.98 1.95  2.44 0.55  0.98 0.66  1.68 0.15  0.62 0.17  0.67 0.19  0.84 2.43  2.82 0.49  0.90

6 6 6 6 6 6 6 6 6 6 6 6

Right (92)

P

5.21  1.89 0.87  0.97 3.92  2.31 1.11  1.14 1.79  2.34 0.64  1.15 0.46  1.34 0.09  0.41 0.05  0.32 0.02  0.17 2.29  2.68 0.55  0.96

.644 .562 .869 .197 .388 .442 .342 .118 .109 .068 .435 .364

MC, medial canthus; ML, medial limbus; MP, mid pupillary line; LL, lateral limbus; LC, lateral canthus; AS, attached span; FM, free margin; , larger than right in statistically; 6, no statistical difference.

however, the OOM was not attached to the periosteum and a fibrofatty tissue was found between the OOM and the periosteum. At 16 mm below the ciliary margin, no attachment of the OOM to the periosteum was observed. A fibrofatty tissue was found between the OOM and the periosteum throughout its course (Fig. 7).

Attachment of the OOM to the Maxilla



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168). For approximately half of all cases (45.6%, 83), the OOM was attached at the MP line. However, it was rarely attached at the LL line (14.3%, 26) or at the LC (4.4%, 8) (Fig. 8). The FM (the distance from the arcus marginalis to the uppermost attachment of the lower OOM) varied according to the location (from 0.10 [0.60] mm at LC to 0.77 [0.90] mm at ME). The AS (the distance from the uppermost attachment of the lower OOM to the lowermost attachment) was widest at the MC (5.35 [2.03] mm) and became gradually thinner at the ML (3.90 [2.37] mm) and the MP (3.90 [2.37] mm) and was thinnest and frail at the LL (0.56 [1.51] mm) and the LC (0.11 [0.53] mm). There were significant differences among the 5 points (P ¼ 0.000 [analysis of variance]) (Tables 1–2, Fig. 9). The AS was wider in men than in women (P < 0.05 [t-test], Table 3); however, there was no difference between the right side and the left side (P > 0.05 [t-test], Table 4).

DISCUSSION Haddock et al2 stated that the palpebral portion of the OOM was rigidly attached to the maxilla, where it takes its origin. The origin of the OOM was an obliquely oriented, dense muscular attachment arising from the maxilla, projecting inferiorly and laterally well below (4–6 mm) the orbital rim and corresponding precisely to the tear trough and the overlying junction between the palpebral and orbital portions of the OOM. Wong et al4 wrote that the OOM origin is several millimeters below the orbital rim (medially, 2 mm; MP, 6 mm; and laterally, 5 mm).

The OOM was almost always attached to the maxilla at the medial epicanthus (100%, 182 sides) and at the ML line (92.3%,

FIGURE 10. Schema of the OOM as seen with a seagull just lifting off from a twig. Top, On the ML, the gull’s feet are still in orbit. Middle, In the MP line, the gull is just taking off from orbit and its wings are spreading. Bottom, On the LL, the gull soars off and its feet are not seen.

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FIGURE 11. The mechanism of making a nasojugal groove. Left, Frontal views; right, parasagittal views at the MP line. Top left and right, In a relaxed state, the nasojugal groove is not evident because the attached portion does not pull the wings. Bottom left and right, While squinting, the OOM, the protractor of the eyelid, contracts and the vertical width shortens, and thereafter, a surface puckering of the delicate periorbital skin appears (arrowhead).

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In our study, the FM (the distance from the arcus marginalis to the uppermost attachment of the lower OOM) varied according to the location (from 0.10 [0.60] mm at the LC to 0.77 [0.90] mm at the ME). It is interesting that Wong et al4 wrote that the ‘‘tear trough ligament’’ was sandwiched between the palpebral and orbital parts of the orbicularis oculi. Although several gross dissections and high-magnification pictures were presented, it was very hard to see the ‘‘tear trough ligament’’ as sandwiched between the palpebral and orbital parts of the orbicularis oculi. Recently, Yang et al5 said that the OOM is linked to the orbital bone through the orbicularis retaining ligament, with multiple branches penetrating the origin of the OOM. A ligament is defined as (1) a band of fibrous tissue that connects bones or cartilage, serving to support and strengthen joints; (2) a double layer of a peritoneum extending from one visceral organ to another; and (3) cordlike remnants of a fetal tubular structure that remain nonfunctional after birth.6 According to its definition, we could not agree with the description that the ‘‘ligament (orbicularis retaining ligament, or tear trough ligament) penetrates a muscle (OOM).’’ In our 3 parasagittal sections, we could not find a ‘‘tear trough ligament’’ sandwiched between the palpebral and orbital parts of the orbicularis oculi. We also could not see the ‘‘orbicularis retaining ligament, with multiple branches penetrating the origin of the OOM.’’ Instead, we observed many connective tissue structures between the muscle bundles of the OOM. At the MP line and the LL line, a fibrofatty tissue was found between the OOM and the periosteum. We noticed that the OOM looks like a seagull just lifting off from a twig. On the ML, the gull’s feet are still in orbit. In the MP

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Origin of Lower Orbicularis Oculi Muscle

line, the gull is just taking off from orbit and its wings are spreading. On the LL, the gull has soared and its feet are not seen (Fig. 10). We think that the mechanism of making a nasojugal groove is as follows. In a relaxed state, the nasojugal groove is not evident because the attached portion does not pull on the wings. While squinting, the OOM, the protractor of the eyelid, contracts and the vertical width shortens, and thereafter, a surface puckering of the delicate periorbital skin appears along with the origin of the OOM (Fig. 11).

ACKNOWLEDGMENT The authors thank Kwan Hyun Youn, PhD ([email protected]), medical illustrator, for his drawings.

REFERENCES 1. Standring S. Gray’s anatomy. 39th ed. Edinburgh, UK: Elsevier; 2005 501–503

2. Haddock NT, Saadeh PB, Boutros S, et al. The tear trough and lid/cheek junction: anatomy and implications for surgical correction. Plast Reconstr Surg 2009;123:1332–1340 3. Ghavami A, Pessa JE, Janis J, et al. The orbicularis retaining ligament of the medial orbit: closing the circle. Plast Reconstr Surg 2008;121:994– 1001 4. Wong CH, Hsieh MK, Mendelson B. The tear trough ligament: anatomical basis for the tear trough deformity. Plast Reconstr Surg 2012;129:1392–1402 5. Yang C, Zhang P, Xing X. Tear trough and palpebromalar groove in young versus elderly adults: a sectional anatomy study. Plast Reconstr Surg 2013;132:796–808 6. Anderson DM, ed. Dorland’s illustrated medical dictionary. 28th ed. Dorland’s illustrated medical dictionary. Philadelphia: WB Saunders; 1994. 925.

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Origin of the Lower Orbicularis Oculi Muscle in Relation to the Nasojugal Groove.

The aim of this study was to clarify the location of the origin of the lower orbicularis oculi muscle (OOM) in relation to the nasojugal groove.In 45 ...
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