The Localization of the Supraorbital Notch or Foramen is Crucial for Headache and Supraorbital Neuralgia Avoiding and Treatment

Authors


Abstract

The aim of this study was to provide the morphological and morphometric data of the supraorbital foramina or notches related to sex, side, and the climatic conditions where the population lived. It was hypothesized that the distribution of the occurrence and location of these openings depends on climatic conditions in which the population lived. Orbits from 866 dried skulls obtained from three climatic regions: warm, temperate, and cold were examined. The examination concentrated on the configuration (notch/foramen) and on the distances to the reference points: nasion, frontomalare orbitale, infraorbital foramen and the superior orbital rim. In 14.3% of cases a smooth supraorbital rim was observed while different variants of the structures were observed in 85.7% of the cases. In cold climatic conditions, supraorbital foramina were found in the highest frequency (35.4%). In warm and temperate climates, the observed frequencies of supraorbital foramen were the lowest (18.8% and 19.9%, respectively). Frequency of supraorbital notches was the lowest of those skulls from a cold climate (44.0%) and the highest in those from a warm climate (59.0%). These results support the hypothesis that the occurrence of the supraorbital notches is greater in populations from warm compared with cold regions. This would provide a greater exit route for the neurovascular bundle and this may be related to the thermoregulatory processes in the supraorbital region. Furthermore, knowledge of precise locations of supraorbital structures is important when a supraorbital nerve block is given, for example, in the treatment of migraine headaches. Anat Rec, 2012. © 2012 Wiley Periodicals, Inc.

INTRODUCTION

Knowledge of the distances from surgically important anatomical landmarks to the supraorbital foramen (SoF) and notch (SoN) may assist surgeons to localize these important maxillofacial openings and to avoid injuring the neurovascular bundle passing through these structures (Knize, 1996; Cutright et al., 2003; Saylam et al., 2003; Agthong et al., 2005; Gupta, 2008; Chrcanovic et al., 2011). It is also important when supraorbital nerve blocks are given, for example, in the treatment of migraine headaches (Levin, 2010).

The aim of this study was to provide the morphometric data of the supraorbital foramina or notches related to sex, side, and the climatic conditions where the population had lived. In previous studies, it has been reported that the position of these anatomical structures vary among genders and ancestry groups (Kimura, 1977; Hanihara and Ishida, 2001). Moreover, the distribution of the occurrence of SoF/SoN and the location of these openings may depend on climatic conditions in which the population lived. If this is the case, then populations from warm climates may have a higher proportion of supraorbital notches than populations from colder regions and thus a higher proportion of foramina as the exit route for the supraorbital neurovascular bundle than other populations. This could represent an adaptation to cold climates and associated thermoregulatory processes in the forehead region. The supraorbital vein, which is more exposed and more prone to heat loss when it passes through supraorbital notch than through supraorbital foramen as well as smaller frontal sinuses in populations from colder regions may have also played role in determining the type of the supraorbital structure in populations from different climatic conditions (Hanson and Owsley 1980; Kondrat 1995; Rae et al. 2011).

Despite the possible significance of the SoF/SoN, little attention has been given to these morphological features in the European populations (Malet et al., 1997; Beer et al., 1998). Therefore, four European skull samples were chosen (Table 1) to investigate bilateral configuration and location of the SoF/SoN with respect to the surgically encountered anatomical landmarks. In this study, we show that these differences could also depend on climatic conditions of these populations.

Table 1. List of populations included, number of individuals, geographic regions, climatic conditions, and current location of samples studied
Morphological sampleNumber of individualsClimatic categoryAverage annual temperatureLatitude rangeDate range (century)Current location
Karelians and Saamis309Cold0°C66–70° North19–20thKunstkamera Museum, St. Petersburg, Russian Federation
Poles151Temperate8°C50–52° North18thDepartment of Anthropology, Wroclaw University, Wroclaw, Poland
Lithuanians205Temperate6°C52–54 °North17–18thDepartment of Anatomy, Histology and Anthropology, Faculty of Medicine, Vilnius University, Vilnus, Lithuania
Italians, Greeks201Warm15°C36–40° North19–20thDepartment of Anthropology, The Museum of Natural History, Vienna, Austria

The supraorbital nerve is prone to traumatic injury, due to its superficial, exposed location (Levin, 2010), that can cause, for example, headaches or supraorbital neuralgias after frontal trauma (Sjaastad et al., 1999, 2005). Supraorbital neuralgia is defined as: (1) pain in the distribution of the SoN, (2) tenderness over the nerve in the supraorbital notch, and (3) abolition of pain by blockade or ablation of the SoN (Headache Classification Committee, 2004; Lipton and Bigal, 2006). Correct diagnosis of these symptoms is crucial in choosing appropriate therapies. Supraorbital neuralgia or migraine can be treated with SoN blockade (Gupta, 2008; Evans and Pareja, 2009; Levin, 2010).

Detailed anatomical knowledge of forehead anatomy, anatomical variants of the supraorbital structures and innervation will help surgeons avoid complications and is important for successful surgical procedures in this area. The forehead is innervated by the supratrochlear and supraorbital nerves, both stemming from the frontal nerve, which is one of the terminal branches of the first division of the trigeminal nerve (cranial nerve V). The frontal nerve runs forward in the superior wall of the orbit. This cutaneous sensory nerve passes between the levator palpebrae superioris muscle and periosteum of the roof of the orbit, then divides into supraorbital and supratrochlear nerves (STNs) that exit the superior edge of the orbit, passing through the notch (supraorbital notch) or foramen (supraorbital foramen), and supplies the medial and lateral aspects of the forehead, respectively, extending as far as the coronoid suture (Bostwick et al., 1995; Moore and Daley, 2006; Fahrenbach et al., 2007). The passage of the nerve through the supraorbital notch or foramen and the exposed location of the nerve on frontal bone render it susceptible to injury.

There are various causes of supraorbital nerve injuries. Symptomatic supraorbital neuralgia cases are usually posttraumatic (Sjaastad et al., 1999, 2005) and less frequently secondary to tumors (Moore et al., 1976; Benvenuti, 1999) and infections (Talmi et al., 1999). Trauma of the nerve might occur as a result of a local anesthetic injection or surgery (Klein and Schmidt, 1991). Also, chronic compression of the supraorbital nerve against the frontal bone may give rise to headaches and has been reported to cause migraines. Compression neuropathy can be caused by anesthesia mask pressure (oxygen and anesthetic masks), where the nasal portion of the mask lies directly over the supraorbital ridge. External pressure, such as caused by a tight headwear and wearing of tightly fitting swimming goggles may be the cause of chronic headaches owing to supraorbital neuralgia (Jacobson, 1983; Pestronk and Pestronk, 1983; O'Brien, 2004).

Some “primary” supraorbital neuralgia may be caused by microtraumas. The supraorbital notch or foramen are the sites where the nerve is confined to a narrow anatomical passageway as well as inside the orbit where the nerve may be indirectly influenced by the eyeball movements. Such localization of the supraorbital nerve may contribute to greater frequencies of compression. Moreover, the supraorbital nerve is accompanied by the supraorbital artery passing through the supraorbital notch or foramen, so, compression of the nerve by vascular congestion could theoretically occur (Caminero and Pareja, 2001).

Headache is a clinical entity that can present both diagnostic and therapeutic challenges. Patients with chronic frontal headache can be successfully diagnosed and treated for neuropathic pain caused by posttraumatic supraorbital nerve injury with a supraorbital nerve block (Antonacie et al., 1997). Correct localization of the supraorbital nerve depends on applying the general rules. So far, the localization of the supraorbital nerve was established by palpating method and guidelines to its location: approximately 2 cm lateral to the STN, which lies just above the eyebrow over its medial border. The supraorbital nerve is blocked by inserting the needle and advancing laterally to the STN and injecting approximately 1–2 cc of anesthetic (bupivacaine or lidocaine, or a mixture of both) (Evans and Pareja, 2009; Massry et al., 2011). The results from the present study show, however, that these rules may not be applicable and reliable to all populations living in different climatic conditions and ancestry groups.

MATERIALS AND METHODS

We analyzed 1732 orbits from 866 dried skulls with known age (63.8% were male and 36.2% were female). The sex of the individuals was determined on the basis of the morphological assessment of the skull (according to the Scoring System for Sexually Dimorphic Cranial Features), as well as according to the standard criteria used in forensic anthropology (Standards of Data Collection) (Buikstra and Ubelaker 1994). The age of the individuals was assessed on the basis of closure of the spheno-occipital synchondrosis as well as cranial suture closure for determining the skeletal ages.

The age of the subjects ranged from 22 to over 70 years. Data were sampled from anthropological collections, divided into three climatic regions: cold, warm, and temperate. Determining the climatic conditions in which the population lived, the average annual temperatures were taken into account (www.weatherbase.com) as well as localization of each sample (latitude range from www.satsig.net) (Table 1).

Temperate climate samples consisted of Wroclaw citizens and to inhabitants of Lithuania (localization between 50 and 55° North latitude). Both collections are held at the Department of Anthropology, Wroclaw University, Poland (N = 151; 18th century samples) as well as at the Vilnius University, Vilnius, Lithuania (17–18th centuries samples; N = 205). Warm climate samples came from Italy and Greece (below 45° North latitude) and currently are held at the Naturhistorishes Museum, Vienna, Austria (N = 201, 19–20th centuries sample). Cold climate samples came from Kola Peninsula (above the Arctic Circle and 66° North latitude) and from the Republic of Karelia (Russian Federation territory, above 64° North latitude). Both collections are held at the Kunstkamera Museum, Sankt Petersburg, Russian Federation (19–20th centuries; N = 309).

The Statistica (version 9.0) was used for the analysis. The frequencies, mean, standard deviation, minimum, and maximum for each of the measurements were assessed. The examination concentrated on the configuration (notch/foramen) and frequencies of these structures for three populations groups from different climatic conditions (warm, temperate, and cold) as well as on the distances to the reference points. Parameters measured bilaterally including minimal distances from medial margin of the supraorbital foramen or notch to anthropological landmarks: nasion (n), frontomalare orbitale (fmo), to the infraorbital foramen (IoF) and superior orbital rim (SOR) (Saller, 1957) (Fig. 1; Table 2). The shape of the supraorbital structure was recorded as a notch or foramen, incomplete foramen, double foramen, or accessory foramen. Multiple foramina were also recorded, with the largest or most prominent being considered as the primary structure for analysis. Comparisons were made between genders, sides, and between the three climatic groups.

Figure 1.

Reference points used for the localization of the supraorbital structures: n = nasion; fmo = frontomalare orbitale; iof = infraorbital foramen; SOR = supraorbital rim.

Table 2. Description of the reference points used for the localization of the supraorbital structures (Saller, 1957)
 Landmark nameAbbreviationDescription
1NasionnThe juncture in the sagittal plane of the frontonasal and internasal sutures
2Frontomalare orbitalefmoThe point where the frontozygomatic suture crosses the inner orbital rim.
3Foramen infraorbitaleIoFLocated below the inferior orbital rim on the facial surface and transmits the infraorbital nerve (a division of cranial nerve 5) and vessels to the face. a passage for the infraorbital nerve and artery
4Superior orbital rimSORUpper margin of the orbit
5Supraorbital foramenSoFSupraorbital structures at superior and medial margin of the orbit in the frontal bone. Lies laterally from the mid-point Connecting maxillofrontale and frontomalare orbitale points.
6Supraorbital notchSoN 

Normal distribution was tested with Shapiro-Wilk test. Metric measurements with normal distributions were analyzed by paired sample t-test for comparisons between sides and unpaired t-sample test for comparisons between sexes and different climatic samples. For non-normally distributed variables, the Wilcoxon signed rank test and Mann-Whitney U-test were used to compare sides and sexes, respectively, and the Kruskal–Wallis test for comparisons between three climatic groups within each of the sexes. For nonmetric observations, X2 nonparametric test for comparing general frequencies in three groups was used. A Wilcoxon test for comparisons between sides and U Mann-Whitney test for comparisons between sexes in each separate climatic group were used. A Kruskal–Wallis test for comparisons between three climatic groups within each sex was also used (Field, 2006; Stanisz, 2006). Differences between groups were considered as significant at P < 0.05.

The data were acquired with the precise tip of the Microscribe G2L (Immersion Corp.), a 3D contact scanner, measuring to the nearest 0.01 mm. The device yields a complete 3D landmark location (Nagasaka et al., 2003). The accuracy of the obtained data was 0.23 mm and interobserver error was 0.036 mm. Most previous research used the midline plane as a reference point (Cutright et al., 2003; Saylam et al., 2003; Agthong et al., 2005; Gupta, 2008; Chrcanovic et al., 2011), but this location is likely to vary among individuals. As a result, we studied two novel reference points, aimed to locate the foramen with fewer disturbances from surrounding structures by using nasion and frontomalare orbitale as reference points. The reason for using this method was the convenience in locating the nasion point in living subjects, thus resulting in a better clinical application of the data as it can also be easy palpated through the skin (Beer al., 1998).

RESULTS

Smooth supraorbital rims were observed in 14.3% of cases and different variants were observed in the remaining 85.7%. At the supraorbital margin, 20 variations and combinations of exit points for the supraorbital nerve were found. From the present result regarding the frequencies of the supraorbital foramen or notch, 33.3% demonstrated bilateral notching, 13.2% bilateral foramina, and 16.8% a notch on one side and a contralateral foramen. Bilateral smooth supraorbital rims occurred in 8.2% of the cases. The remainder of the cases (28.5%) presented various combinations of analyzed structures (Table 3).

Table 3. Bilateral frequencies of the observed structures
Righr supraorbital rimLeft supraorbital rimN%
NotchNotch28833.3
foramenForamen11413.2
NotchForamen748.6
foramenNotch718.2
Smooth supraorbital rimSmooth supraorbital rim718.2
NotchSmooth supraorbital rim485.5
NotchIncomplete foramen424.8
Incomplete foramenNotch333.8
Smooth supraorbital rimNotch283.2
Incomplete foramenIncomplete foramen263.0
ForamenIncomplete foramen232.7
ForamenSmooth supraorbital rim161.8
Incomplete foramenForamen111.3
Smooth supraorbital rimForamen91.0
Smooth supraorbital rimIncomplete foramen30.4
f. add.Notch20.2
Incomplete foramenSmooth supraorbital rim20.2
f.add.Incomplete foramen20.2
Foramenf.add10.1
Notchf.add.10.1

When samples were analyzed separately, according to climatic living conditions of each population, supraorbital notches occurred more often than foramina but with characteristic dependence on climatic conditions. The frequency of supraorbital notches was the lowest in populations from cold climatic conditions (44.0%) and the greatest in populations from warm climate (59.0%). Supraorbital foramina were found in highest frequency (35.4%) in populations from cold climates. In populations from temperate and warm climates, the frequency of supraorbital foramina were the lowest (18.8 and 19.9%, respectively) (Pearson's Chi2 = 50.768; P = 0.000) (Table 4).

Table 4. Frequencies of the supraorbital foramina and notches depending on the climatic conditions for three populations
Climatic conditionsNotchForamenForamen add.Incomplete foramenSmooth supraorbital rimDamagedTotal
WarmN2378035032 402
%59.019.90.812.48.0  
TemperateN363134265148 712
%51.018.80.39.120.8  
ColdN272219255682618
%44.035.40.38.911.00.3 
TotalN872433717024821732
%50.425.00.49.814.30.1 

Statistically important differences were observed between populations from cold and warm climates (P = 0.0127) as well as between cold and temperate climatic conditions (P = 0.0011) (Kruskal–Wallis test). Statistically significant differences were found only for male populations from cold and temperate climates (P = 0.0006) and between male samples from cold and warm climate (P = 0.0123, Kruskal–Wallis test). For female populations, no statistically significant differences were observed (Table 5). No statistically significant differences in occurrences of the supraorbital structures between both sexes in each of three analyzed populations were observed (Mann-Whitney U test, P > 0.05). Additionally, no differences for right and left sides in frequencies in each of three analyzed populations were observed (with Wilcoxon signed rank test, P > 0.05 in all three populations).

All metric variables were non-normally distributed (Shapiro-Wilk test, P < 0.05). Mean distances and ranges of distances to the three reference points are shown in Table 6. In all populations, distances to nasion were longer for the right side than for left. For the other reference points, the mean left side distances were longer than for the right side. The distance to the nasion reference point was the longest for the population from warm climate conditions (mean for right and left side 25.3 mm) and the shortest for the population from cold climate conditions (mean for right and left side 24.3 mm). For distances to frontomalare orbitale (31.7 mm and 30.6 mm, respectively) and infraorbital foramen (42.9 mm and 42.5 mm, respectively) reference points, similar relations were noticed. In case of the measurement to the supraorbital rim, a reverse correlation was observed. In the population from a cold climate, supraorbital structures were localized in a higher position (3.6 mm) that in a warm climate (2.9 mm).

Table 5. Kruskal-Wallis Test P values for differences in frequencies of the supraorbital foramina and notches in three populations in male and female separately
Male FemaleWarmTemperateCold
  • a

    Statistically significant difference.

Warm 1.0000000.012271a
Temperate1.000000 0.000590a
Cold1.0000000.418184 

Comparing samples from three different climatic conditions (Table 7), statistically important differences were found between all samples for distances to the nasion point for the right side (warm to temperate and warm to cold climate: P = 0.0004 and 0.0031, respectively) and for distance to the nasion point for the left side between warm and temperate samples (P = 0.0435) and between warm and cold climate sample as well (P = 0.0334). For the distance to FMO for the right side differences were found for samples from the warm and cold climates (P = 0.00002) and for temperate and cold climates (P = 0.0007). For the left side, differences were found only between the warm and cold climate samples (P = 0.0401). For the distance between SoF and infraorbital foramen, differences were only found for the left side between cold and warm climates (P = 0.0492). Statistically significant differences were also found for distances to the SOR for the right side between cold and warm climates (P = 0.0156) and between temperate and warm climates (P = 0.0120) (Kruskal–Wallis test). In female samples, only one statistically significant difference between three climatic samples was found: between cold and warm climate for the distance to infraorbital foramen for the left side (P = 0.0452). In male samples, differences in distances between populations were found for the distance for the right side to the nasion point between populations from cold and warm climates as well as between temperate and warm climates (P = 0.0134 and P = 0.0002, respectively). For the left side, the only difference found was for temperate and warm climatic conditions (P = 0.0419). For the right side, differences in the distance to the frontomalare orbitale reference point between cold and warm sample and between cold and temperate (P = 0.027 and P = 0.0001, respectively) were observed. Additionally, there were significant differences for the distance from the right supraorbital rim to the supraorbital foramen (P = 0.0011, Kruskal–Wallis test).

Table 6. Mean and ranges for distances to the reference points: nasion, frontomalare orbitale, infraorbital foramen, and supraorbital rim (in mm)
Climate categorySupraorbital foramen or notch to nasion (ranges) SDSupraorbital foramen or notch to frontomalare orbitale (ranges) SDSupraorbital foramen or notch to infraorbital foramen (ranges) SDSupraorbital foramen to supraorbital rim (ranges) SD
RightLeftMeanNRightLeftMeanNRightLeftMeanNRightLeftMeanN
Warm25.89 (19.572–38.269)24.76 (17.228–36.556)25.336831.78 (21.649-46.298)31.58 (18.299-39.914)31.737542.25 (26.444-50.349)43.47 (35.710-52.821)42.93822.77 (1.90-6.70)2.986
SD 2.81SD 3.24SD 3.08SD 3.44SD 3.48SD.46SD 4.19SD 2.88SD 3.64SD 2.42SD 2.62
Temperate24.92 (17.843–36.250)24.07 (14.766-41.290)24.5 SD 3.7452831.14 (18.680-39.247)31.15 (20.860-49.490)31.247042.48 (24.370-54.720)42.88 (34.718-52.733)42.74602.96 (1.79 4.74)3.24 (1.69-5.19)3.188
SD 3.81SD 3.36 SD 3.15SD 3.26SD 3.20SD 3.15SD 3.19SD 3.36SD 1.64SD 2.01SD 2.29
Cold24.57 (16.155–38.600)-23.95 (16.431-38.307)24.345530.27 (20.938-38.477)30.96 (20.875-43.799)30.644442.34 (27.072-49.621)42.69 (29.910-51.783)42.54363.42 (1.50-6.84)3.69 (1.63-8.80)3.6172
SD 3.60SD 3.83SD 3.75SD 3.13SD 3.19SD 3.17SD 2.91SD 3.06SD 3.06SD 1.25SD 1.62SD 1.43
Total25.20 (16.155-38.600)24.22 (14.766-41.290)24.7135131.06 (18.680-46.298)31.21 (18.299-49.490)31.1128942.36 (24.370-54.720)43.00 (29.910-52.821)42.712783.08 (1.50-6.84)3.45 (1.63-8.80)3.3346
SD 3.51SD 3.61SD 3.59SD 3.28SD 3.31SD 3.29SD 3.54SD 3.07SD 3.33SD 1.80SD 1.75SD 2.76

In all three analyzed populations together, differences between right and left sides for measurements to nasion point and to frontomalare orbitale were observed. For the distance to IoF, one difference for the population from the warm climate was found. For the distance to supraorbital rim, only one difference occurred, for temperate climate and the distance to infraorbital foramen was statistically significant only in the population from warm climate conditions (Wilcoxon signed rank test, P < 0.05).

Mean distances for three population samples between males and females are shown in Tables 8–10. The differences in mean distances from SoF/SoN to the nasion point between male and female for both sides (right and left) were insignificant in all three populations. Statistically significant differences were found in distances between SoF/SoN and FMO between sexes for right as well as for left sides in populations from cold and temperate climate conditions (P < 0.05). For populations from cold climatic conditions, we also found statistically important differences for the distance from SoF/SoN to IoF for right and left sides (P < 0.05). In the population from warm climatic conditions, no significant differences between males and females were observed (Mann-Whitney U-test, P < 0.05) (Table 10).

Table 7. Kruskal–Walis P-values for distances in three populations from different climate conditions
Distance WarmTemperateCold
N-SOF PWarm0.0004390.003062
Temperate0.0004391.000000
Cold0.0030621.000000
N-SOF LWarm0.0434670.033367
Temperate0.0434671.000000
Cold0.0333671.000000
SOF-FMO PWarm0.7840150.000017
Temperate0.7840150.000697
Cold0.0000170.000697
SOF-FMO LWarm0.0930820.040141
Temperate0.0930821.000000
Cold0.0401411.000000
SOF-IOF PWarm1.0000000.906152
Temperate1.000000-1.000000
Cold0.9061521.000000-
SOF- IOF LWarm0.1433600.049234
Temperate0.1433601.000000
Cold0.0492341.000000
SOF –supraorbital rim PWarm0.0527560.000011
Temperate0.0527560.414427
Cold0.0000110.414427-
SOF –supraorbital rim LWarm0.4578250.105682
Temperate0.4578251.000000
Cold0.1056821.000000
Table 8. Mean distances to the reference points for population from cold climate conditions (in mm)
 MaleFemaleP
 MeanSDNMeanSDN
n-sof.P25.053.7513724.863.40940.687998
n-sof.L24.223.9513023.583.65940.217868
sof-mfo.P30.882.9213429.393.22920.000396
sof-.mfo.L31.433.0912830.283.23900.008451
sof-.iof.P42.673.0913441.842.57900.035234
sof-.iof.L43.193.0212541.982.98870.004329
odl P3.611.36553.161.05390.078718
odl L3.941.73493.281.34290.080057
Table 9. Mean distances to the reference points for population from temperate climate conditions (in mm)
 MaleFemaleP
 MeanSDNMeanSDN
n-sof.P24.933.8213724.693.641260.609485
n-sof.L23.913.8914024.123.491140.644300
sof-mfo.P32.312.8012430.243.081110.000000
sof-.mfo.L31.962.7612330.253.571020.000069
sof-.iof.P42.753.1912242.063.831080.137920
sof-.iof.L43.043.1312042.563.261000.262882
odl P2.818.52233.09710.66250.165484
odl L3.012.79173.411.23230.154457
Table 10. Mean distances to the reference points for population from warm climate conditions (in mm)
MaleFemale P
MeanSDNMeanSDN
n-sof.P25.972.7916825.102.94160.238411
n-sof.L24.693.0216825.545.05160.313892
sof-mfo.P31.843.4916831.172.96160.457460
sof-.mfo.L31.673.4417430.643.84170.247859
sof-.iof.P42.154.2317443.293.78170.285277
sof-.iof.L43.392.8217444.283.47170.227934
odl P2.32.54743.041.48120.368875
odl L2.9522

DISCUSSION

Proportions of bilateral distribution of the supraorbital structures presented here are consistent with a previous study where the highest frequencies occurred for bilateral supraorbital notches than for foramina. Malet et al. (1997) in research on Caucasians, observed bilateral notches in 65%, bilateral foramen in 20.0%, and a notch and ipsilateral foramen in 10.0%. In another study, Beer et al. (1998) showed bilateral notches in 70% of a Caucasian sample. In the Webster et al. study (1986), bilateral notches occurred in 49.07%, bilateral foramen in 25.93%, and a notch and ipsilateral foramen in 25%.

Bilateral notches occurred also in the Trivedi et al. study (2010) of Gujarati Indians in 35.62%; bilateral foramen in 21.45%; and a notch on one side and contralateral foramen occurred in 8.36%. In a study by Sinha (1978) of 400 Indian skulls, bilaterial notches were observed in 44.25%, bilateral foramina in 18.25%, and a notch and contralateral foramen in 12.55%. Apinhasmit et al. (2006) observed in Thai skulls bilateral notches in 50%, bilateral foramina in 17%, and in 33% there was notch for one side and foramen contralaterally. In a study conducted by Cheng et al. (2006) in a Chinese population, bilateral notches were observed in 40.2%, bilateral foramen in 24.8%, and notch on one side and foramen on other in 24.8%. Chung et al. (1995) in the study of photographs of 124 Korean skulls, reported that the supraorbital notch occurred in 69.9% and was found more frequently than the supraorbital foramen (28.9%).

The results from the present study indicate lower frequencies of all analyzed structures; however, this is consistent with the general statement that supraorbital notches occur with higher frequency than supraorbital foramina in all compared samples. The present result support our hypothesis that in the population from the cold climate supraorbital foramina were found in the highest frequency (35.4%) and supraorbital notches in the lowest frequency (44.0%) (Table 4). The present data would suggest that the characteristics of supraorbital structures are associated with different climatic conditions.

These observations are consistent with Hanihara and Ishida (2001), where they have reported that Northeast Asians and North Americans from colder, arctic climatic conditions have higher frequencies of the supraorbital foramina than other populations.

The mean distances in the anatomical landmarks in the three populations also support our assumption that the localization of the supraorbital structure is associated with climatic conditions. In the present study, the distances to nasion (24.7 mm) point were similar to those studied in Thai (25.14 mm) as reported in the Apinhasmit study (2006), the Agthong (2005) study (24.7 mm), and in Chinese in the Cheng et al. study (2006) (25.33 mm). However, these distances were made to the midline, not to the nasion point as in the present study. In the Malet et al. (1997) study of Caucasians, measurements were made to nasion points and were much lower than in the present study (18.32 mm). Saylam et al. (2003) in a study of a Turkish population reported that this distance was 25.23 mm. Chung et al. (1995) in studies from photographs of Korean skulls stated, that the average distance from the median plane to the center of the supraorbital notch/foramen was 22.7 mm. Additionally, mean distances of SoN/SoF to nasion in the present study were lower from those studied in Brazilians (Chrcanovic et al., 2011), Europeans (Beer et al., 1998) and in the studies conducted by Aziz et al. (2000) (26.4 mm).

These variations might be caused by ancestry differences that confirm previous reports (Hanihara and Ishida, 2001) as well as climatic influences on the morphology of the human skull. Higher localization of the supraorbital neurovascular bundle in foramina than in notches as well as higher localization of the supraorbital foramen in populations from cold climates than in population from warm climate may be the result of the climate on living conditions of each population. These observations would suggest that clinically palpating the SoN alone is not sufficient in locating the supraorbital neurovascular bundles in many cases. Clinicians should be aware that neurovascular bundles might exit through SoF well above the supraorbital rim, and that combination of notches and foramina in the same skull are possible. It is difficult during surgical intervention or anesthetic procedures to exactly identify the midline of the skull. Therefore, the use of a new reference point as nasion, which could be easier localized in living subjects, and the mean 25.20 mm for right side and 24.22 mm for left side (Table 6) may be a better landmark for performing a coronal approach in European populations. For the FMO reference point, we should take into account the distance of approximately 31 mm (31.06 for the right side and 31.21 for the left) and for the distance to the supraorbital rim we should take approximately 3.08 mm for the right and 3.45 mm for the left side.

The present study supports the presence of gender differences in the positions of SoN/SoF, reported in different populations (Agthong et al., 2005), but only for distances to the frontomalare orbitale for the right and left side for population from cold and temperate climates as well as for the distance to IoF for both sides in populations from cold climates. From the present results, these distances were longer in males than in females. Surgeons should be aware of such differences in the localization of these foramina. The mean position did vary in different ancestry groups. These data demonstrated that the most common position of the SoF is approximately 24.7 mm to the nasion point, 31.1 mm to FMO point and 42.7 mm to IoF reference point and 3.3 mm to the supraorbital ridge when it comes to supraorbital foramen.

Knowledge of the distance from the supraorbital rim may be useful in identifying critical structures during dissection as well as during other surgical procedures (Kleier et al., 1983). The closest determination of the SoF location should be considered when designing access incisions to the orbital vault and rim and planning regional blockage as well as when IoF is localized. Localization of the IoF is often based on the distances between SoF, thus incorrect localization of the SoF may result in incorrect localization of the IoF as well. Kleier et al. (1983) suggested a technique that involves infiltrating an anesthetic solution in the area defined by dropping a vertical line from the palpable SoN to about 10–15 mm below the infraorbital rim. According to the present results, it may be effective to infiltrate an anesthetic solution in the area that is 42.36 mm for right side and 43.00 mm for left side (Table 6), in comparison to 44.95 mm below the SoN/SoF in the same vertical line in Kleier study (1983) and 42.92 mm in Aziz et al. study (2000).

Results support our hypothesis that the localization and frequency of the SoN/SoF depends on climatic conditions and ethnicity. Surgical procedures of the supraorbital region are delicate and precise. It is obvious that a detailed knowledge of relevant anatomy is essential to attain appropriate surgical results (Cuzalina and Holmes, 2005). The precise identification of SoN/SoF is crucial for both diagnostic and clinical procedures (Chung et al., 1995; Malet et al., 1997). It is also of great importance with the rising popularity and frequency of endoscopic brow lift procedures with limited visibility (Ramirez, 1994) and other invasive procedures (Reisch et al., 2003). Damaging the neurovascular bundle may result in paresthesia or anesthesia (Ramirez, 1994; Malet et al., 1997; Gupta, 2003; Cuzalina and Holmes, 2005; Massry et al., 2011). Knowledge of the exact location of supraorbital foramen/notch is important when a supraorbital block is given, for example, in the treatment of migraine headaches (Ramirez, 1994; Caputi and Firetto, 1997). However, the palpating method to localization the SoN/SoF may not be sufficient (Beer et al., 1998; Trivedi et al., 2010; Chrcanovic et al., 2011). The measurements to new reference points (nasion, frontomalare orbitale, foramen infraorbitale and distance to the supraorbital rim) may better help surgeons to locate these anatomical structures. We should be aware of different combinations of SoN/SoF in the same skull and in skulls from different climatic conditions. The anatomy of supraorbital foramina or notches did vary between the populations. Moreover, different data between sides and genders have been reported and this should be considered when applying the anatomical variation data to an individual subject.

The present study adds information to the literature concerning morphology of the SoF/SoN, especially in European populations from different climatic conditions. Differences in occurrence of the different variant of the supraorbital structures could be connected with thermoregulatory processes and harsh climate influence on human skull morphology. Specifically, the differences noted here may represent a morphological adaptation to limit heat loss from veins passing through supraorbital structures in populations from cold climate. This can be facilitated by a higher localization of the neurovascular bundle and displacement deeper into the frontal bone and thus, localization of this bundle in the foramen and not in the notch.

As aforementioned, the supraorbital structures were located in a higher position in the population from cold climate regions. Frontal sinuses may also play an important role in shaping the supraorbital structures. In populations from colder regions, smaller frontal sinuses were found (Hanson and Owsley 1980; Kondrat 1995; Rae et al. 2011). This allows a medial and deeper embedding of the supraorbital structures into the frontal bone, what was also shown in the present study. For example, the distance to nasion reference point was the shorter in the population from cold climate zones (24.3 mm) compared to those in warm climate zones (25.3 mm). The distance to the SOR also supports our assumption: 2.9 and 3.6 mm in warm and cold climate, respectively.

The knowledge of the distances from surgically encountered anatomical landmarks in the present study may assist surgeons to localize these important maxillofacial openings and avoid injuring the neurovascular bundles and facilitate surgical, local anesthetic, and other invasive procedures. Extra care should be taken during surgical procedures in supraorbital region because population variations have been described. Although this was out of scope of this particular research, it is worth mentioning, that supraorbital structures may also play an important role in forensic identification, because of their specific individual variants. This may become more important with newer medical imaging modalities. The results from the present study are of practical clinical value but also should encourage further studies into the morphological adaptations that have occurred in human populations exposed to different prevailing climatic conditions.

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