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. 2022 Dec 6;45(1):43–53. doi: 10.1007/s00276-022-03051-1

The sphenoidal emissary foramina prevalence: a meta-analysis of 6,369 subjects

Maria Piagkou 1,✉,#, Michael Kostares 1,#, Fabrice Duparc 2, Panagiotis Papanagiotou 3, Constantinus Politis 4, George Tsakotos 1, Nikos Pantazis 5, Konstantinos Natsis 6
PMCID: PMC9849305  PMID: 36472634

Abstract

Purpose

To estimate the prevalence of the sphenoidal emissary foramina (SEF), and the effect of possible moderators on it.

Methods

A systematic online literature search was conducted. The pooled prevalence with 95% confidence intervals was estimated. Outlier and influential analyses were performed. The presence of small-study effect and publication bias were evaluated. Moderator analyses were executed to investigate the effect of the specimens’ continent of origin, type of study (dried skull or imaging), probing for the evaluation of SEF patency (conduction and instruments used), side dominance (bilateral or unilateral), morphometric data [SEF diameter, distances SEF–Foramen ovale (FO) and SEF–Foramen spinosum (FS)], and the methodology used for the morphometric measurements (caliper, DICOM Viewer, and image analysis software) on the estimated prevalence.

Results

In total, 6,460 subjects from 26 studies were included in the meta-analysis. The overall SEF prevalence was estimated as 38.1%. The heterogeneity was high and statistically significant. No indications of publication bias and small-study effect were identified. The conducted subgroup analyses did not yield statistically significant differences in the SEF prevalence between groups, except of the type of side dominance. Both results of the univariable and multivariable regression analyses showed the association of the unilateral dominance with a decrease in the reported SEF prevalence.

Conclusion

The identification of more unilateral than bilateral foramina in a given cohort is associated with a decrease in the reported crude SEF prevalence. Laterality-specific estimates should be established for a precisive estimation of the emissary foramina prevalence.

Keywords: Foramen Vesalius, Sphenoidal emissary foramen, Prevalence, Meta-analysis, Laterality-specific prevalence

Introduction

The constant foramina (foramina ovale and spinosum, FO and FS) are located in the posterior part of the greater wings of the sphenoid bone. FO transmits the mandibular nerve and occasionally the accessory meningeal artery and the lesser superficial petrosal nerve. FS is perforated by the middle meningeal artery and the meningeal branch of the trigeminal nerve [12]. Occasionally, anteromedially or anteriorly to the FO [19, 31], a small sized foramen—the so-called sphenoidal emissary foramen (SEF) or foramen of Vesalius (FV) can be unilaterally or bilaterally identified. SEF has not been identified in any other primates than human [40]. As per its content, SEF transmits a sphenoidal emissary vein (SEV) connecting the pterygoid venous plexus to the cavernous sinus [24]. Therefore, it is important in neurosurgical procedures, such as in FO cannulation for trigeminal nerve rhizotomy, as well as pathway of spreading of extracranial infections into the cavernous sinus [22, 25, 35]. The SEF occurrence varies widely among different studies’ samples [13].

The current meta-analysis provides a more precise estimation of the SEF prevalence and pinpoints the variables associated with the SEF presence.

Materials and methods

Search strategy

A systematic literature search was conducted by two independent assessors in August 2022 using Publish or Perish software [15]. Through this application, all available databases except for the Web of Science (Crossref, GoogleScholar, OpenAlex, PubMed, Scopus, and Semantic Scholar) were scanned using combinations of the following keywords: [“foramen Vesalius”, “sphenoidal emissary foramen”, “presence”, “occurrence”, “prevalence”, “incidence”)]. Notably, in Semantic Scholar and OpenAlex, only single keywords were used since both databases’ application programming interfaces did not support the use of Boolean operators. After duplicates’ removal, each publication’s reference list was manually scanned for potentially non-identified studies. The systematic literature search flowchart (Fig. 1) is based on the PRISMA 2020 Statement [29].

Fig. 1.

Fig. 1

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Flow chart depicting the systematic search results from the relevant studies' identification and selection

Criteria for study selection and data inclusion and extraction

All original studies reporting data regarding SEF prevalence were included with no restriction on language or publication date. Case reports, review articles, letters to the editor, conference abstracts, doctoral thesis, studies with no full-text or detailed abstracts available, and articles that could not be cross-verified by multiple secondary sources were excluded. Out of each publication, the extracted data included the authors, year of publication, continent of origin (Europe, Asia, and America), type of data (dried skulls and imaging), probing for evaluating SEF patency (yes or no), instrument used for probing (bristle, wire, and other), total sample, reported SEF frequency (total, bilateral, and unilateral), type of dominance (bilateral: when the bilateral to unilateral foramina ratio was greater than 1, otherwise, unilateral), morphometric data (SEF diameter, SEF–FO, and SEF–FS distances), and the methodology used for the morphometric measurements (caliper, DICOM Viewer, image analysis software). In publications not mentioning the continent of origin, the country where the study originated from, was eventually recorded and in case of an article written in a non-Latin language (e.g., Russian), the full paper was downloaded and translated using the Google Translate website (https://translate.google.com). Additionally, in manuscripts where only the bilateral or unilateral percentages were reported, the respective frequencies (bilateral and unilateral frequency) were calculated by converting each percentage to integers with no decimal approximation.

Quality assessment

The quality assessment was performed according to the Anatomical Quality Assessment (AQUA) tool [16], a tool consisting of 25 questions and dividing into 5 areas: 1. Objectives and Subject Characteristics, 2. Study Design, 3. Methodology Description, 4. Descriptive Anatomy, and 5. Results Reporting. For each domain, where all questions were replied affirmatively, the risk of bias was rated as 'low', otherwise as 'high'. Study quality was defined as ‘high’ if at low risk of bias in all five domains, ‘moderate’ if at low risk of bias at least in three domains, and otherwise as ‘low’.

Statistical analysis

Statistical analysis was carried out using RStudio (version: 2022.7.1.554) software (RStudio Team (2022)). RStudio: Integrated Development for R. RStudio, PBC, Boston, MA for MacOS. The DerSimonian and Laird random-effects model was used to estimate the pooled prevalence and its respective 95% confidence intervals (CI). No logit or double arcsine transformation were made since the observed proportions identified across studies were between 0.2 and 0.8 [21, 37]. Heterogeneity presence across studies was estimated by constructing a forest plot and tested using the Cochran’s Q statistic and its respective p value. The Higgins I2 statistic and its respective 95% CI were used for quantifying the magnitude of true heterogeneity in effect sizes. An I2 value of 25%, 50%, and 75% indicated low, moderate, and high heterogeneity. To detect studies that overly contributed to the heterogeneity, a Baujat plot [2] was created. To determine if the potential outlying studies, as evaluated in this plot, were also influential, screening for externally studentized residuals with z-values larger than two in absolute value and leave-one-out diagnostics were performed [38]. With the outlying and influential studies removed, the pooled prevalence, its’ respective 95% CI, and the substantial heterogeneity were re-evaluated through moderator analyses. In the conducted subgroup analyses, the following covariates were evaluated: continent of origin, type of data, probing, sample size, dominance, study quality, and measurements. As per the sample size, all manuscripts were divided into two categories (small and large studies) based on the median sample size (n = 239 subjects). In the performed univariable regression analyses, except of the aforementioned covariates, the SEF diameter, as well as the SEF–FO and SEF–FS distances were assessed as per their relationship with the respective effect sizes. Moreover, the presence of interrelated moderators was checked to avoid potential multicollinearity issues prior the conduction of the multivariate regression analysis. Due to the limited availability of data about the SEF diameter, and the SEF-FO, and SEF-FS distances in the given dataset, they were not used in this analysis. To detect the presence of publication bias, a Doi plot and a funnel plot were created. The asymmetry of each plot was estimated by calculating the LFK index [9] and Egger’s tests’ p value, respectively. Additionally, to detect the presence of the small-study effect, the phenomenon that smaller studies may show different, often larger effects than large ones [33], a funnel plot of the prevalence against the sample size was constructed and regression-based Egger’s test was estimated. The arithmetic difference between percentages was expressed in percentage point units [39]. Unless otherwise stipulated, the statistical significance was established at p = 0.05 (two-tailed).

Results and discussion

Search results and characteristics of the included studies

A total of 26 studies (n = 6,460 subjects); 23 dried skull (n = 5,590 subjects) and 4 imaging (n = 870 subjects) were included. Thirteen studies (48.2%) were conducted in Asia, nine studies (36.3%) in America, and five (18.5%) in Europe. The majority of articles evaluated the SEF patency (15 studies, 55.6%). Out of them, seven studies (46.6%) reported the use of wires, three (20.0%) the use of bristles, and five (33.4%) the use of other materials, such as metallic probes or endodontic files. The 66.7% of the included studies were estimated as moderate quality and the remaining ones as high quality. The 51.9% of the studies that referred to the SEF had calculated its anteroposterior diameter by utilizing the use of calipers (six studies, 42.9%), DICOM viewers (three studies, 21.4%) or image analysis software (five studies, 35.7%). A list of the included studies is presented in Table 1.

Table 1.

Main characteristics and data outcome of the included studies

Authors Year Continent Study type Probing Total sample SEF frequency Dominance Study size Study Quality Conduction of measurements SEF morphometry (in mm)
T B/L U/L SEF diameter SEF–FO SEF–FS
Alves and Deana [1] 2017 America Dried skulls No 178 57 43 14 Bilateral Small Moderate Yes (caliper) 2.19
Bayrak et al. [2] 2018 Asia Imaging No 317 89 22 67 Unilateral Large Moderate Yes (DV) 2.74 2.26 11.29
Boyd [3] 1930 Europe Dried skulls No 1500 548 221 327 Unilateral Small Moderate No
Berlis et al. [4] 1992 Europe Dried skulls No 60 22 9 13 Unilateral Large Moderate Yes (DV)
Chaisuksunt et al. [5] 2012 Asia Dried skulls Yes (wire) 377 61 16 45 Unilateral Large High Yes (IAS) 1.59 2.42
Costa do Nascimento et al. [6] 2018 America Dried skulls No 194 36 12 24 Unilateral Small Moderate Yes (caliper)
Dogan et al. [7] 2014 Asia Dried skulls No 31 15 5 10 Unilateral Small Moderate Yes (caliper) 2.46 3.61
Ginsberg et al. [9] 1994 America Imaging No 123 98 60 38 Bilateral Small Moderate No
Görürgöz and Paksoy [10] 2020 Asia Imaging Yes (wire) 260 190 110 80 Bilateral Large High Yes (DV) 1.75 1.39 10.32
Gupta et al. [12] 2005 Asia Dried skulls Yes (bristle) 35 15 8 7 Bilateral Small Moderate No
Gupta et al. [13] 2014 Asia Dried skulls Yes (bristle) 200 68 28 40 Unilateral Small Moderate No
Jadhav et al. [15] 2016 Asia Dried skulls Yes (bristle) 250 72 44 28 Bilateral Large High No
Kale et al. [16] 2009 Asia Dried skulls Yes (other) 347 156 87 69 Bilateral Large High No
Leonel et al. [18] 2019 America Dried skulls Yes (other) 1000 468 254 214 Bilateral Small High No
Imaging No 170 77 32 45 Unilateral Large High No
Maletin et al. [20] 2020 Europe Dried skulls No 26 16 14 2 Bilateral Small Moderate No
Martinez et al. [21] 2014 America Dried skulls No 53 18 6 12 Unilateral Small Moderate No
Murlimanju et al. [23] 2015 Asia Dried skulls Yes (other) 78 29 13 16 Unilateral Small High No
Natsis et al. [24] 2018 Europe Dried skulls Yes (wire) 195 78 42 36 Bilateral Large High Yes (IAS) 2.71 2.31
Nayak et al. [25] 2018 Asia Dried skulls Yes (other) 30 9 6 3 Bilateral Small High Caliper (yes) 1.26 1.80
Ozer and Govsa [26] 2014 Asia Dried skulls No 172 60 16 44 Unilateral Small Moderate Yes (IAS) 0.97 2.38 10.59
Raval et al. [28] 2015 Asia Dried skulls Yes (wire) 150 61 29 32 Unilateral Small Moderate Yes (caliper) 1.05
Reymond et al. [29] 2005 Europe Dried skulls Yes (wire) 100 17 5 12 Unilateral Small Moderate Yes (IAS)
Rossi et al. [30] 2010 America Dried skulls No 80 32 11 21 Unilateral Small Moderate Yes (caliper) 1.52 2.16
Sharma and Garud [31] 2011 Asia Dried skulls Yes (wire) 50 31 22 9 Bilateral Small Moderate No
Shinohara et al. [32] 2010 America Dried skulls Yes (wire) 400 135 62 73 Unilateral Large Moderate Yes (IAS) 0.71 2.57 11.24
Toledo junior et al. [33] 2016 America Dried skulls Yes (other) 84 35 14 21 Unilateral Small Moderate No
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T total, B/L bilateral, U/L unilateral, DV DICOM Viewer, IAS image analysis software

Prevalence of the sphenoidal emissary foramen (SEF)

A random-effects model analysis yielded an initial overall SEF prevalence of 39.8% (95% CI 34.0−45.7) (Fig. 2).The estimated heterogeneity was statistically significant (p < 0.001), and of high magnitude (I2 = 95.8%; 95% CI 92.9–97.7). The Baujat plot and the influence diagnostics are presented in Figs. 3 and 4. According to them, even though several studies were initially identified as outliers, the diagnostics indicated that only the Ginbserg et al. [10] study had an influential effect. The forest plot illustrating the results of the leave-one-out analyses is presented in Fig. 5. After the exclusion of the relevant study, the new pooled SEF prevalence was estimated at 38.1% (95% CI 32.8–43.4) with a reduction of 1.2% in the I2 being noticed (I2 = 94.6%; 95% CI 93.2–95.8).

Fig. 2.

Fig. 2

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Forest plot evaluating the calculated prevalence of the sphenoidal emissary foramina (SEF) using random-effects model

Fig. 3.

Fig. 3

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Diagnostic plot (Baujat plot) for the detection of heterogeneity sources in meta-analytic data. On the horizontal axis, the contribution of each study to the overall Q-test statistic is displayed

Fig. 4.

Fig. 4

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Visual representation of the influence diagnostics for each of the included studies. Influential studies are marked as red dots. Abbreviations used—rstudent: studentized deleted residuals; dffits: DFFITS values; cook.d: Cook’s distances; cov.r: covariance ratio; tau2.del: estimated τ2 values; QE.del: estimated Cochran’s Q values

Fig. 5.

Fig. 5

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Forest plot displaying the re-calculated pooled effects, with one study omitted each time, using the leave-one-out method. The further a box deviates from the reference line, the more pronounced the impact of the corresponding missing study will be on the original summary proportion

Publication bias and small-study effect

Both the produced Doi and funnel plots (Fig. 6) for the assessment of presence of publication bias were assessed as asymmetric implying that bias might be present. However, the estimated LFK index (LFK index = 0.78) and the Egger’s test p value for the quantification of each plots’ asymmetry, respectively, were not deemed consistent with publication bias. As per the small-study effect, according to the data presented in Table 2 as well as on the interpretation of the produced funnel plot (Fig. 6) and the respective Egger’s test p value, the SEF prevalence was not moderated by the sample size. Therefore, no small-study effect was present.

Fig. 6.

Fig. 6

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Depiction of the produced plots for the detection of publication bias (plots a, b) and small-study effect presence (plot c). The estimation of each plot’s asymmetry was performed by calculating the LFK index for plot (a) and Egger’s tests’ p value for plots (b) and (c)

Table 2.

The results of the subgroup analysis on the differences of the subjects’ continent of origin, type of data, probing, sample size, laterality, and study quality on the estimated prevalence

Predictor Moderator (subgroup) k Prevalence (95% CI) QM QE
Continent of origin Europe 5 36.2% (26.7–45.8) 0.845  < 0.0001
America 8 36.4% (28.4–44.4)
Asia 13 39.9% (29.7–50.1)
Type of data Imaging 3 48.8% (20.1–77.5) 0.401  < 0.0001
Dried skulls 23 36.4% (31.7–41.0)
Probing No 11 35.8% (30.4–41.1) 0.508  < 0.0001
Yes 15 39.2% (30.7–47.6)
Instrument used Wire 7 40.2% (23.3–57.0) 0.941  < 0.0001
Bristle 3 32.5% (26.7–38.3)
Other 5 43.5% (39.3–47.7)
Dominance Unilateral 16 33.1% (28.1–38.1) 0.016  < 0.0001
Bilateral 10 46.0% (36.8–55.3)
Sample size Small 17 37.5% (31.9–43.2) 0.842  < 0.0001
Large 9 38.6% (29.3–48.0)
Study quality Moderate 17 35.7% (31.4–40.1) 0.473  < 0.0001
High 9 40.4% (28.4–52.5)
Measurements No 12 41.5% (36.9–46.2) 0.198  < 0.0001
Yes 14 34.8% (25.6–44.0)
Instrument used Caliper 6 34.0% (24.6—43.5) 0.084  < 0.0001
DICOM Viewer 3 46.0% (13.3—78.8)
Image analysis software 5 28.3% (18.2—38.3)
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In bold text, the statistically significant findings are being noted

k number of studies combined, QM p value of the test of moderators, QE p value of the test of residual heterogeneity

Moderator analysis

The results of the subgroup analyses are summarized in Table 2. The SEF prevalence varied significantly only by the type of dominance (p = 0.016). The results of the performed regression analyses display the existence of a statistically significant, and a marginally non-significant association of the reported SEF prevalence with dominance (p = 0.005), and type of data (p = 0.060), respectively (Table 3). Specifically, according to the multivariable regression results, the unilateral dominance was associated with a 13.0 percentage points decrease in the reported SEF prevalence. In other words, when a sample of dried skulls is examined, the reported SEF prevalence will be 13.0% smaller if the frequency of the identified unilateral foramina exceeds the one of the bilateral. This finding highlights the necessity of the simultaneous recording and reporting of the unilateral and bilateral SEF prevalence (laterality-specific prevalence). The performed moderator analyses explained 32.3% of the residual heterogeneity (R2 = 32.3%).

Table 3.

The output of the univariable and multivariable linear meta-regression analyses performed for the association of the sphenoidal emissary foramen (SEF) presence with the studied variables

Univariable models Multivariable model
Estimate p value 95% CI Estimate p value 95% CI
Continent of origin
 America (ref.)
 Asia 0.03 0.597 (− 0.09; 0.15)
 Europe 0.01 0.956 (− 0.15; 0.16)
Type of data
 Dried skulls (ref.)
 Imaging 0.12 0.106 (− 0.03; 0.27) 0.13 0.060 (− 0.01; − 0.26)
Probing
 No (ref.)
Yes 0.02 0.768 (− 0.09; 0.12)
Instrument used
 Bristle − 0.02 0.778 (− 0.21; 0.16)
 Wire 0.03 0.705 (− 0.11; 0.16)
 Other 0.02 0.705 (− 0.13; 0.18)
Dominance
 Bilateral (ref.)
 Unilateral − 0.13 0.010** (− 0.22; − 0.03) − 0.13 0.005** (− 0.22; − 0.04)
Study sample size
 Large (ref.)
 Small − 0.01 0.880 (− 0.12; 0.10)
Study Quality
 High (ref.)
 Moderate − 0.04 0.482 (0.32; 0.49)
Measurements
 No (ref.)
 Yes − 0.08 0.140 (− 0.18; 0.02)
SEF diameter 0.02 0.787 (− 0.13; − 0.17)
SEF–FO distance − 0.06 0.527 (− 0.27; − 0.15)
SEF–FS distance − 0.35 0.194 (− 1.12; − 0.43)
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In bold text, the statistically significant findings are being highlighted

Ref reference category, 95% C.I. 95% confidence intervals, SEF diameter sphenoidal emissary foramen’s anteroposterior diameter (measured in mm), SEF–FO distance distance between sphenoidal emissary foramen and foramen ovale (measured in mm), SEF–FS distance distance between sphenoidal emissary foramen and foramen spinosum, ** strong statistical association

Study’s limitations

First, it should be noted that the unidentified heterogeneity remains on moderate levels. This indicates that the reported summary estimates must be interpreted with caution. Moreover, the small number of imaging studies and articles from various geographic locations (e.g., Europe), as well as the lack of a “gold standard” for measuring foramina dimensions and relative distances should be considered. Therefore, more effort should be made toward this direction.

Conclusion

The SEF prevalence is estimated at 38.1%. The unilateral dominance is associated with a decrease in the SEF prevalence. Therefore, laterality-specific estimates should be established and followed for the estimation of the emissary foramina prevalence.

Abbreviations

FO

Foramen ovale

FS

Foramen spinosum

FV

Foramen of Vesalius

SEF

Sphenoidal emissary foramen

SEV

Sphenoidal emissary vein

CI

Confidence intervals

SEF–FO

Sphenoidal emissary foramen to foramen ovale distance

SEF–FS

Sphenoidal emissary foramen to foramen spinosum distance 

Author contributions

ΜΚ: literature search, manuscript writing, formation of methodology, and statistical meta-analysis; GT: literature search and manuscript editing; MP: formation of methodology, quality assessment, manuscript editing, and supervision; CP: quality assessment, manuscript editing, and supervision; NP: statistical meta-analysis and supervision; PP, FD, KN: manuscript editing and supervision.

Funding

Open access funding provided by HEAL-Link Greece. Open access funding was provided by the Hellenic Academic Libraries Link (HEAL-Link). The authors did not receive support from any organization for the submitted work.

Data availability

Literature and Rstudio data are available if requested.

Declarations

Competing interests

The authors declare no competing interests.

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Ethical approval

This declaration is not applicable.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Maria Piagkou and Michael Kostares equally contributed to the paper.

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