Anatomical Study of the Zygomaticotemporal Branch Inside the Orbit

The location of the opening of the zygomaticotemporal branch (ZTb) of the zygomatic nerve inside the orbit (ZTFIN) has significant surgical implications. This study was conducted to locate the ZTFIN and investigate the variations of the ZTb inside the orbit. A total of 20 sides from 10 fresh frozen cadaveric Caucasian heads were used in this study. The vertical distance between the inferior margin of the orbit and ZTFIN (V-ZTFIN), the horizontal distance between the lateral margin of the orbit and ZTFIN (H-ZTFIN), and the diameter of the ZTFIN (D-ZTFIN) were measured. The patterns of the ZTb inside the orbit were classified into five different groups: both ZTb and LN innervating the lacrimal gland independently (Group A), both ZTb and LN innervating the lacrimal gland with a communicating branch (Group B), ZTb joining the LN without a branch to the lacrimal gland (Group C), the ZTb going outside the orbit through ZTFIN without a branch to the lacrimal gland nor LN (Group D), and absence of the ZTb (Group E). The D-ZTFIN V-ZTFIN H-ZTFIN ranged from 0.2 to 1.1 mm, 6.6 to 21.5 mm, 2.0 to 11.3 mm, respectively. The number of sides in Groups A, B, C, D, and E were 13 sides (65%), three sides (15%), none (0%), two sides (10%), and two sides (10%), respectively. Such anatomical knowledge might reduce complications following surgery in and around the ZTb.


Introduction
The zygomaticotemporal branch (ZTb) of the zygomatic nerve, which is a branch of the maxillary division of the trigeminal nerve, runs along the lateral wall of the orbit. It passes through the zygomaticotemporal foramen (ZTF) and then travels in the temporal fossa [1]. It has a communicating branch with the auriculotemporal and facial nerves [2][3]. Inside the orbit, many anatomical depictions have shown a communicating branch between the ZTb and the lacrimal nerve (LN) [4]. The ZTb carries sensory fibers to the temporal region and receives parasympathetic fibers from the pterygopalatine ganglion that are destined to innervate the lacrimal gland directly or indirectly through the LN. According to Scott et al.,however,60.6% of the cadaveric heads did not have any communicating branches between the ZTb and LN [5]. In addition, the ZTb has variations in its course inside the orbit. Most studies of the ZTb have investigated the course in the temporal fossa in terms of surgery of the temporal fossa and temporal approaches [2,4,6]. From the surgical point of view, the location of the opening of the ZTb inside the orbit (ZTF IN ) is also important and the existence of the communicating branch might impact the surgical procedure. Thus, a more detailed anatomy of the ZTb inside the orbit is necessary to better understand and reduce complications. Therefore, this study was conducted to locate the ZTF IN and investigate the variation of the ZTb inside the orbit.

Materials And Methods
A total of 20 orbits from 10 fresh frozen cadaveric Caucasian heads were used in this study. The specimens were derived from two males and eight females and the age at death ranged from 63 to 90 years (mean age: 78.0±7.9 years old). In the supine position, a skin incision was made along the inferior to lateral margin of the orbit. First, the periosteum inside the orbit was elevated superiorly and medially to identify the ZTF IN   Two clinical anatomists performed all dissections and measurements. Dissections were carried out under a surgical microscope (OPMI CS NC31, Carl Zeiss, Oberkochen, Germany), and measurements were made with a microcaliper (Mitutoyo, Kanagawa, Japan) with a resolution of 0.01 mm and an accuracy value of ±0.025 mm. The measurements were performed three times by each observer (for a total of six times for each measurement) and then averaged. The present study protocol did not require approval by the ethics committees in our institutions, and work was performed in accordance with the requirements of the Declaration of Helsinki (64th WMA General Assembly, Fortaleza, Brazil, October 2013).

Results
The total number of ZTF IN   For the patterns of the ZTb inside the orbit, 13 sides (65%) were classified as Group A, three sides (15%) as Group B (Figure 2), none (0%) as Group C, two sides (10%) as Group D, and two sides (10%) as Group E ( Table 2). Of these, two sides in Group A had no ZTF IN but ZTb directly innervated the lacrimal gland without a communicating branch to the LN. Additionally, the other two sides in Group E had an unusual branch, which arose from the LN and passed through the ZTF IN after giving rise to a branch to the LN.

ZTb and the LN innervated LG and had a communicating branch (arrowheads).
LG

Discussion
Previous anatomical studies of the ZTF have revealed morphological features of the foramina on the lateral surface of the zygomatic bone [7][8]. Kim et al. investigated the ZTF using microcomputed tomography (micro-CT) and found that the bony canal often bifurcates inside the zygomatic bone [9]. However, the bony canals identified in dry skulls or on CT could include not only the nerves but also vessels. In the present study, only the nerves passing through the foramina were focused on and dissected using a surgical microscope. It has been traditionally taught that the lacrimal nerve does not carry parasympathetic fibers to the lacrimal gland but the ZTb does, so that the communicating branch between the ZTb and LN exists in most cases. However, recently, Scott et al. reported that a communicating branch was found in less than 40% of the cases [5]. Compared to Scott et al.'s study, Group A was 65% in our study (60.6% in Scott's study), Group B was 15 % in our study (36.4% in Scott's study), and Group C was 0% in our study (3% in Scott's study). Neither Group D nor Group E was classified in Scott et al.'s study. Group D was 10% and had no innervation to the lacrimal gland. Group E was 10% without any ZTb but the lacrimal nerve passed through the ZTF IN . The pathways of the parasympathetic fibers described in textbooks do not explain the innervation in Groups D and E because, in these groups, the lacrimal gland only received its nerve supply from the LN. In such cases, the LN should carry the parasympathetic fibers but immunohistochemistry is necessary to prove this.
The human zygomatic bone has one to three ossification centers. These appear in the eighth week of gestation and fuse at about the 22 nd week [11]. The embryological origin of the variations of the ZTF may be due to the variations of its ossification centers and this might result in various numbers of foramina. Based on anatomical studies of the mandible, Iwanaga et al. speculated that the mental foramen is formed by the addition of bone around the nerve bundles proximal to the branching point, and accessory mental foramina are formed by bone addition peripheral to the branching point [12][13]. This could be applied to the formation of multiple ZTF IN . If the bone addition occurs around the ZTb bundles before giving rise to branches, theoretically, only one ZTF IN would be formed. However, if the bone addition occurs after giving off branches, it might form an additional zygomaticotemporal foramen.

Conclusions
Our results revealed a variation in the distribution of the ZTb. Occasionally, the ZTb did not innervate the lacrimal gland where its only innervation was via the LN. An immunohistochemical examination is now required to identify parasympathetic fibers inside the ZTb and LN in order to better understand the innervation of the lacrimal gland.

Additional Information Disclosures
Human subjects: Consent was obtained by all participants in this study. This study involves cadaveric human specimens. . Animal subjects: All authors have confirmed that this study did not involve animal subjects or tissue. Conflicts of interest: In compliance with the ICMJE uniform disclosure form, all authors declare the following: Payment/services info: All authors have declared that no financial support was received from any organization for the submitted work. Financial relationships: All authors have declared that they have no financial relationships at present or within the previous three years with any organizations that might have an interest in the submitted work. Other relationships: All authors have declared that there are no other relationships or activities that could appear to have influenced the submitted work.