Abstract
Introduction
The zygomaticofacial/temporal/orbital nerve is a terminal branch of the zygomatic nerve and exits the orbit through zygomatic foramina. The nomenclature in the literature varies with some studies identifying all three foramina on the malar surface of the zygoma, while others describe each along different aspects of the zygoma. In this study, foramen on the malar surface of the zygoma are termed zygomatic foramen, and the authors describe anatomic variations in the position and number of these foramina in an African American population.
Methods
Sixty-two African American skulls from the Hamann-Todd collection of the Cleveland Museum of Natural History were studied. The primary outcome was the number of zygomatic foramina on the malar surface of the zygomatic bone. Secondary outcomes included the location of foramina relative to the orbital rim and the frontozygomatic suture. Mean and standard deviation were used to describe measurements. Chi-squared and Wilcoxon Signed-Rank tests were used to analyze measurements between left and right hemicrania.
Results
The average number of foramina was 1.98 ± 0.93. More foramina were found on the right (2.13 ± 0.98) when compared to the left (1.68 ± 0.79; p = 0.001). The average distance between the lateral-most and medial-most foramina was 9.7 ± 5.0 mm. The distance from the orbital rim to the lateral foramen was 8.4 ± 4.2 mm, and distance from the orbital rim to the medial foramen was 7.7 ± 2.1 mm. The frontozygomatic suture was 22.9 ± 3.9 mm from the lateral foramen and 27.9 ± 3.6 mm from the medial foramen.
Discussion
The locations of the foramina in relation to the frontozygomatic suture and orbital rim were consistent with other populations. However, in this African American population, more zygomatic foramina were noted compared to previously published results in Korean, Indian, Brazilian, and West Anatolian populations. Surgeons should be cognizant of zygomatic foramina in this population to reduce potential neurovascular complications.
Introduction
Terminal trigeminal nerve branches perforate the zygomatic bone through the zygomaticofacial/temporal/orbital foramina (hereto referred to as zygomatic foramina) to innervate the skin overlying the cheek and temporal fossa. Awareness of the location of the zygomatic foramina is important in procedures such as orbitozygomatic osteotomy, inferior wall fracture repair, endoscopic subperiosteal midface lift, and neurotoxin injections1–4. Complications of injury to the neurovascular bundles within the zygomatic foramina include mid-face paresthesias, dysesthesias, neuralgiform pain, as well as intraoperative bleeding and postoperative hematoma5–8. Understanding the anatomic variations of this structure should improve surgical planning and reduce complications.
Racial differences in the anatomy of the zygomatic foramina have been described. The number of foramina can vary between 0 to 59, 10. Korean and Brazilian studies showed a relative predominance of single or double zygomatic foramina, while four foramina were found in 5.5% of Western Anatolian skulls3, 11, 12. In archeologic studies, lack of zygomatic foramina was more prevalent in Argentinian skulls, and a description of a Paranthropus robustus skull from Drimolen, South Africa found two zygomatic foramina8, 13. We sought to determine the anatomic variations of zygomatic foramina in African American skulls.
Methods
The authors utilized the Hamann-Todd skull collection at the Cleveland Museum of Natural History. Upon initial receipt of these skulls each was dried, preserved, and stripped of soft tissues and periosteum by the Human Anthropology staff. African American skulls were selected based on catalogue numbers from the initial compilation of the collection. One hundred and twenty-four sides of 62 African American skulls (42 male and 20 female) were examined.
Measurements included the number of zygomatic foramina for the right and left hemicrania and the distance between the medial-most and lateral-most foramen. Location of the zygomatic foramina was determined in relation to the orbital rim and the frontozygomatic suture (Figure 1). A line perpendicular to the tangent of the orbit was drawn from the medial-most foramen to the orbital rim and measured. The distance between the orbital rim and lateral-most foramen was also measured. Finally, we measured the distance between the frontozygomatic suture, at the orbital rim, to the lateral-most and the medial-most foramen (Figure 1). All measurements were obtained by YZ using electronic digital calipers.
Figure 1.
A. Distance between the frontozygomatic suture, at the orbital rim, to the lateral-most (FZ-L) and the medial-most foramen (FZ-M).
B. Distance between the orbital rim and lateral-most foramen (OR-L) and medial-most foramen (OR-M).
Means and standard deviations were reported for continuous variables. Statistical analyses were performed using JMP Pro software (version 12; Cary, NC). Chi-squared analyses was used to compare frequency of one foramina in right and left hemicrania. Wilcoxon Signed Rank test was used to compare average number of foramina in right versus left hemicrania. P < 0.05 significance level was assumed for all tests. Data obtained from hemicrania with one foramen were analyzed in conjunction with measurements from the lateral-most foramen in hemicrania with multiple foramina.
Results
One hundred and twenty-four sides of 62 African American skulls (42 male and 20 female) were examined. Average age at death was 51.0 years, (range, 18 – 89 years; SD = 29.0 years). Damage to the zygoma led to exclusion of three left hemicrania.
The number of zygomatic foramina ranged from 0 to 5 on the right and 0 to 4 on the left hemicranium (Figure 2). Of 62 right-sided measurements, 1 (1.6%) had no discernible foramen, 17 (27.4%) had one foramen, 22 (35.4%) had two foramina, 18 (29%) had three foramina, 3 (4.8%) had four foramina, and 1 (1.6%) had five foramina. Of 59 left-sided measurements, 2 (3.4%) had no discernible foramen, 26 (44.1%) had one foramen, 29 (49.2%) had two foramina, 2 (3.4%) had three foramina, and 3 had four foramina (Table 1).
Figure 2.
Variation in number of zygomatic foramina in African American skulls.
Table 1.
Distribution of the number of foramen in left and right hemicrania. Counts provided, total of 62 right hemicrania and 59 left hemicrania measured.
| Right | Left | Total | |
|---|---|---|---|
| Average # foramina | 2.13 ± 0.98 | 1.68 ± 0.79 | 1.98 ± 0.93 |
| 0 foramen | 1 | 2 | 3 |
| 1 foramina | 17 | 26 | 43 |
| 2 foramina | 22 | 29 | 51 |
| 3 foramina | 18 | 2 | 20 |
| 4 foramina | 3 | 3 | 6 |
| 5 foramina | 1 | 0 | 1 |
Average number of foramen in all hemicrania was 1.98 ± 0.93 (Table 1). There were more foramina on the right side (2.13 ± 0.98) when compared to the left (1.68 ± 0.79, p=0.001), but no significant difference in number of right hemicrania with one foramina, when compared to the left (p=0.13). The average distance between medial-most and lateral-most foramen in hemicrania with multiple foramina was 9.7 ± 5.0mm (right: 10.1 ± 4.9mm, left: 9.3 ± 5.4mm) (Table 2).
Table 2.
Location of zygomatic foramen, right and left hemicrania. Measurements are average ± standard deviation. ZF = zygomatic foramen; FZ = frontozygomatic suture.
| Right | Left | Total | |
|---|---|---|---|
| # hemicrania | 62 | 59 | 110 |
| Distance between medial ZF and lateral ZF | 10.1 ± 4.9* | 9.3 ± 5.4* | 9.7 ± 5.0 |
| Distance between orbital rim to lateral ZF | 7.9 ± 2.8 | 9.0 ± 5.3 | 8.4 ± 4.2 |
| Distance between orbital rim to medial ZF | 7.7 ± 2.4* | 7.8 ± 1.8* | 7.7 ± 2.1 |
| Distance between FZ suture to lateral ZF | 22.8 ± 4.1 | 23.1 ± 3.8 | 22.9 ± 3.9 |
| Distance between FZ suture to medial ZF | 28.3 ± 4.0* | 27.4 ± 2.9* | 27.9 ± 3.6 |
n=25
For all hemicrania, the average distance from the orbital rim to the sole or lateral-most foramen was 9.7 ± 5.0 mm (right: 7.9 ± 2.8 mm, left: 7.8 ± 1.8 mm). The distance to the medial-most foramen was 8.4 ± 4.2mm (right: 7.7 ± 2.4mm, left: 9.0 ± 5.3). The average distance from the lateral-most foramen to the frontozygomatic suture at the orbital rim was 22.9 ± 3.9mm (right: 22.8 ± 4.1mm, left: 28.3 ± 4.0mm). The distance to the frontozygomatic suture was 27.9 ± 3.6mm from the medial-most foramen (right: 28.3 ± 4.0mm, left: 27.4 ± 2.9mm) (Table 2).
Discussion
The neurovascular structures passing through the zygomatic foramina may be injured iatrogenically during surgery; alternately, subperiosteal dissection or cancer resection in this region requires transecting these structures. Understanding the number, location and racial variations of the foramina may minimize complications and improve the efficiency of surgical dissection in this region.
During embryologic facial development, the zygomatic nerve becomes trapped in mesenchyme at various points along its course in the orbit or within the zygoma as it divides9. This contributes to the morphological variations in the number and location of zygomatic foramina and may offer a biologic explanation for the varying number of zygomaticofacial foramina seen in this and other studies. Another potential embryologic explanation for varying number of zygomatic foramina lies in the potential for one to three ossification centers of the zygoma14, 15.
This group of African American skulls showed a variation in the number of foramina between 0 and 5. An absence of a zygomatic foramen was recently described and was found in 2.4% of the hemicrania in this study16. This variant was less prevalent in our population than in studies of West Anatolia (15.6%), Aryo-Dravidian (21.8%) and Korean (9%) populations (Table 3)3, 9, 12. The occurrence of two foramina in this African American cohort (41.4%) was much higher than previous studies of other populations (up to 30%)3. This suggests that African Americans have a greater number of zygomatic foramina requiring extra caution when manipulating this area surgically.
Table 3.
Variation in number of zygomatic foramina across studies. Total number of hemicrania examined and percentage of skulls for each foramina count. Population studied as described by study authors. Population unspecified in Martins et al, 2003 and Loukas et al, 2008, assumed to be mixed.
| This study | Martins et al, 200310 | Mangal et al, 20049 | Hwang et al, 20073 | Loukas et al, 20086 | Aksu et al, 200912 | Del Neri et al, 201411 | |
|---|---|---|---|---|---|---|---|
| # hemicrania | 120 | 102 | 330 | 110 | 400 | 160 | 302 |
| 0 foramen | 2.4 | 21.6 | 21.8 | 9 | 39 | 15.6 | 18.9 |
| 1 foramen | 34.6 | 50 | 44.9 | 50.9 | 42 | 44.4 | 44 |
| 2 foramina | 41.1 | 23.5 | 27.9 | 30 | 16 | 28.1 | 28.5 |
| 3 foramina | 16.1 | 3.9 | 5.1 | 9 | 7 | 6.3 | 8 |
| 4 foramina | 4.8 | 1 | 0.3 | 0.9 | 1 | 4.4 | 0.7 |
| 5 foramina | 0.8 | 0 | 0 | 0 | 0 | 1.3 | 0 |
| Population | African American | Unspecified | Aryo-Dravidian | Korean | Unspecified | West Anatolia | Brazilian |
Other factors contributing to the results include the method of measuring foramina and nomenclature of zygomaticofacial/temporal/orbital foramina used in previous studies. Methods of examining the zygoma include digital photographs and image analysis software, direct examination of the dry skull, and micro-CT6, 9, 12. Kim et al used micro-CT to assess number and the path of the foramen through the zygoma17. They compared their results to a previous study of Korean skulls examined in a similar manner to Mangal et al9, 18. They found a greater average number of zygomaticofacial foramen compared to a previous study of Korean skulls (2.2 vs 1.7), but both Korean studies had a higher average number of foramina than reported by Loukas et al6. Despite using similar methodologies of examining dry skulls, there was also a lower prevalence of absent foramen in the Korean population than Aryo-Dravidian populations9, 18. This suggests methodology contributes to variation in number of foramina, but there are also racial differences.
The average number of foramina was 1.98 ± 0.93 in this African American population. While higher than previous studies, this is similar to results found in a recent micro-CT study of Koreans where an average of 2.2 foramina per zygomatic bone was reported17. While previous studies suggest no significant difference in the average number of zygomaticofacial foramina between right and left hemicrania, we found that the right side contained significantly more (2.13 ± 0.98) zygomatic foramina than the left side (1.68 ± 0.79)12. This is of unclear significance; data to support potential explanations such as individual handedness were not available.
Distance between the lateral-most and medial-most zygomaticofacial foramen was 9.7 ± 5.0 mm, which was slightly farther than the previously cited 7mm (range 1–13 mm)10. Distance from the orbital rim to the sole or lateral foramen was 9.7 ± 5.0 mm, and distance to the medial foramen was 8.4 ± 4.2mm. This is similar to findings from other populations, which found distances ranging from an average of 5.9 ± 1.4mm to 11mm (range 5–22mm)6, 12. Average distance from the frontozygomatic suture to the lateral foramen (22.9 ± 3.9mm) and medial foramen (27. 9 ± 3.6mm) was also similar to studies of other populations3, 10.
While dissection often requires transecting the neurovascular structures within the zygomatic foramina, this can result in hypesthesia, paresthesias, intraoperative bleeding, and postoperative hematoma formation. These structures can be avoided during many surgeries in the region, such as zygomaticomaxillary approaches to fracture repair, parallel osteotomy of the medial zygomatic body in malarplasty, and a variety of cosmetic midface procedures5, 18. Although the foramina locations were similar, this African American population showed greater number of zygomatic foramina compared to previous populations. Based on our findings and those of others, care should be taken in a 1.5cm2 area starting 5mm below the inferolateral orbital rim when performing subperiosteal dissection in African American patients. This area accounts for the larger number of zygomatic foramina and the distance between the medial-most and lateral-most foramen seen in this patient population. Understanding the number, location, and racial variations of these landmarks may improve surgical efficiency and reduce complications.
Acknowledgments
Financial support– This study was supported in part by the NIH-NEI P30 Core Grant (IP30EY025585-01A1) and Unrestricted Grant from The Research to Prevent Blindness, Inc, awarded to the Cole Eye Institute.
Footnotes
Proprietary interest statement– none of the authors have any conflict of interest to disclose.
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