Annals of Anatomy 238 (2021) 151789 Contents lists available at ScienceDirect Annals of Anatomy journal homepage: www.elsevier.com/locate/aanat RESEARCH ARTICLE Anatomic mapping of the collateral branches of the external carotid artery with regard to daily clinical practice Rosana Cobiella a,1 , Sara Quinones a,1 , Paloma Aragones a,c , Xavier León d , Anto Abramovic b,e , Teresa Vazquez a , José Ramón Sanudo a , Eva Maranillo a , Lukasz Olewnik f , Clara Simon de Blas g , Ian Parkin h , Marko Konschake b,∗ a Department of Anatomy and Embryology, School of Medicine, Complutense University of Madrid, Madrid, Spain b Department of Anatomy, Histology and Embryology, Institute of Clinical and Functional Anatomy, Medical University of Innsbruck (MUI), Innsbruck, Austria c Department of Orthopedics, Hospital Universitario Santa Cristina, Madrid, Spain d Department of ORL, Hospital de la Santa Creu i Sant Pau, UAB, Spain e Department of Neurosurgery, Medical University of Innsbruck (MUI), Innsbruck, Austria f Department of Anatomical Dissection and Donation, Medical University of Lodz, Poland g Department of Computer Science, Universidad Rey Juan Carlos I, Madrid, Spain h University of St. Andrews, School of Medicine, Scotland, United Kingdom a r t i c l e i n f o a b s t r a c t Article history: Background: To identify the anatomical variations of the main branches of the external carotid artery Received 28 April 2021 (lingual, facial, occipital, ascending pharyngeal and sternocleidomastoid), giving information about the Received in revised form 8 June 2021 calibers and origins with the aim of creating a new classification useful in clinical practice. Accepted 8 June 2021 Material and methods: 193 human embalmed body-donors were dissected. The data collected were ana- Available online 30 June 2021 lyzed using the Chi2 test. The results of previous studies were reviewed. Results: The majority of the anterior arterial branches (superior thyroid, facial and lingual artery) were Keywords: observed with an independent origin, respectively, classified as pattern I (80.83%, 156/193). In 17.62% External carotid artery Arterial variations (34/193) a linguofacial trunk, pattern II, has been observed, only in 1,04% (2/193) a thyrolingual trunk, Interventional radiology pattern III, has been found and in one case (1/193, 0.52%) one thyrolinguofacial trunk, pattern IV, was Vascular surgery found. Depending on the posterior branches (occipital and ascending pharyngeal), four different types could be determined: type a, the posterior arteries originated independently, type b, the posterior arteries originated in a common trunk, type c, the ascending pharyngeal artery was absent, type d, the occipital artery was absent. Conclusion: Anatomical variations in these arteries are relevant in daily clinical practice due to growing applications, e.g., in Interventional Radiology techniques. Knowledge of these anatomical references could help clinicians in the interpretation of the carotid system. © 2021 The Author(s). Published by Elsevier GmbH. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). 1. Introduction for the patient’s life (Hollinshead, 1954), entailing one of the main causes of morbidity and, above all, mortality. Furthermore, in the Nowadays, the anatomical knowledge of the carotid vascular field of Interventional Radiology, it is not currently limited to diag- axis is important from a diagnostic as well as from a therapeutic nosis, but also extends to the endoluminal therapeutic approach to point of view in diverse medical fields e.g., Otolaryngology, Inter- vascular pathology. In this case, in a subtraction radiological tech- ventional Radiology and Vascular Surgery. A major injury of the nique, which enhances the arterial vessels by means of a contrast great cervical vessels during surgery can have direct consequences agent, all the external anatomical references are lost except for the bone limits. Therefore, the anatomical domain of the vascu- lar elements is essential for a clear identification of each vessel in Interventional Radiology, especially as a preoperative evaluation ∗ Corresponding author at: Institute of Clinical and Functional Anatomy, Medical for techniques such as extracranial-intracranial bypass procedures University of Innsbruck (MUI), Müllerstr. 59, 6020 Innsbruck, Austria. and carotid endarterectomies (Germans and Regli, 2014; Rajamani E-mail address: Marko.konschake@i-med.ac.at (M. Konschake). 1 Denotes co-first authorship. and Chaturvedi, 2011). https://doi.org/10.1016/j.aanat.2021.151789 0940-9602/© 2021 The Author(s). Published by Elsevier GmbH. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). R. Cobiella, S. Quinones, P. Aragones et al. Annals of Anatomy 238 (2021) 151789 Anatomic variability of the external carotid artery has been reported in previous literature with an incidence of 2.5%–21% (Adachi and Kihara, 1928; Gluncic et al., 2001; Lucev et al., 2000; Mata et al., 2012; Ozgur et al., 2008; Sanjeev et al., 2010; Shintani et al., 1999; Zumre et al., 2005). To date, 2 previous studies referred to a classification of the branches of the carotid arterial axis into arterial patterns (Livini, 1903a, b). Previously, we studied the anatomical variations of the supe- rior thyroid and superior laryngeal arteries (Vazquez et al., 2009). Therefore, the aim of this study was to complete the identification for all anatomic variations within the main branches of the exter- nal carotid artery and to establish a new classification for simple clinical handling. 2. Material and methods A total sample of 193 human embalmed body-donors (386 hemi-necks) from the Department of Anatomy, University of Cam- bridge, UK, were dissected by preclinical medical students and Fig. 1. Right lateral view of Area II after decline the sternomastoid muscle (carotid recorded during a period of four years. triangle). Dissection of the main collateral arteries of the external carotid artery and We have undertaken this study with a sample that previously its relationships with the sympathetic trunk, vagus nerve, hypoglossal nerve and has been partially dissected by medical students. Most of the internal laryngeal nerves. students did not dissect the suprahyoid region, however, some The concept of Area II is clinical used in ENT surgery, is the suprahyoid region behind the digastric muscle and occupied by the internal jugular vein, external carotid artery touched and cut some branches of the ECA. Due to this circum- and accessory, vagus and hypoglossal nerves. stance, some of them are partially deteriorated. Even so, 386 hemi Ijv, internal jugular vein, St: superior thyroid artery, ila: internal laryngeal artery, necks were dissected. The results found were out of a total of 207, Iln: internal laryngeal nerve, La: lingual artery, Fa: facial, Oa: occipital artery. Ph: although in some cases (due to failures in previous dissections) the ascending pharyngeal artery, X: vagus nerve, XII: hypoglossal nerve. number of sample size was lower. Therefore, these cases were not included in the present study. The main sample considered was a 3. Results total of 207 hemi necks. Detailed dissections of arteries were done by experienced anatomists. Firstly, the origin and calibers of the main collateral arteries The individuals had given their written consent to body dona- (lingual, facial, occipital, ascending pharyngeal and sternoclei- tion and use of their bodies for scientific and educational purposes domastoid) were studied (Fig. 1). Secondly, a new classification prior to death. According to National Law, scientific institutions (in of the branches of the external carotid artery was devel- general Institutes, Departments or Divisions of Medical Universi- oped while comparing our findings with those published ties) are entitled to receive the body after death mainly by means previously. of a specific legacy, which is a special form of last will and testament. No bequests are accepted without the donors having registered 3.1. Lingual artery their legacy and been given appropriate information upon which to make a decision based upon written informed consent (policy The lingual artery was the largest artery that originated immedi- of ethics); therefore, an ethics committee approval was waived ately cranial to the superior thyroid artery. The investigation of this (Konschake and Brenner, 2014). artery was performed in 207 hemi-necks. The artery was observed The gender distribution was 74 male and 91 female body- arising from four different levels: external carotid artery (164/207, donors, with an age range of 60–103 years. Clinical histories were 79.23%), common origin in form of an arterial trunk (37/207, 17.4%) available; no case contained any reference to previously performed either with the superior thyroid artery, with the facial artery or vascular surgical intervention. with both of them, carotid bifurcation (2.41%) and the common The dissections were completed and distances between main carotid artery (0.48%) (Fig. 2). The localization of the artery’s ori- collateral branches and external diameters were measured with gin was variable, the anterior surface of the carotid being the most digital calipers (Mitutoyo Absolute Digimatic Caliper, UK). These common in 76.6% of cases (Fig. 3), followed by the anterome- measurements were independently verified by two experienced dial (14.3%), medial (6.5%), anterolateral (1.3%), and lateral (1.3%) anatomists. side. The initial descriptive data presentation was performed using In our sample, 37 trunks were found: 34/37 linguofacial trunks a Windows Excel sheet (Microsoft Office, Version 1908, Microsoft, (91.89%) (Fig. 4 B), 2/37 thryrolingual trunks (Fig. 4A) and 1/37 Inc., Redmond, WA, USA), the subsequent statistical analysis was thyrolinguofacial trunk (rare variation included in (Vazquez et al., performed with SPSS (IBM SPSS Statistics, version 24.0, IBM 2009)). Corporation). After initial testing for normal distribution using Linguofacial trunks were found in 40.54% (15/37) on the left- Kolmogorov–Smirnov test, variances between individual groups hand side originating from the external carotid artery. On the right compared with the population were analyzed using Chi2 test. P side, two thyrolingual trunks (2/37, 5.4%) were found, one of them values of <0.05 were considered statistically significant. originating from the common carotid and the other from the exter- Following the measurements and statistical evaluation, the nal carotid. The rest of the arterial trunks on the right side were results were compared with previously published studies. This linguofacial trunks (19/37, 51.35%) arising at the level of the exter- resulted in a new classification system with special regard to clin- nal carotid artery in the majority of cases, except one starting from ical practice and usability. the carotid bifurcation. In five cases the linguofacial trunks were 2 R. Cobiella, S. Quinones, P. Aragones et al. Annals of Anatomy 238 (2021) 151789 Fig. 2. Frequency origin of the lingual, facial and occipital artery. Fig. 3. Position at the artery in the case of the ascending pharyngeal, occipital, facial and lingual. registered bilaterally. Compared to an isolated origin of the lingual In two cases, the lingual artery originated at the level of the com- artery, the common arterial trunk showed a 0.7 cm higher origin mon carotid artery, one in isolation and the other in the form of a with no significant difference (p > 0.05). thyrolingual trunk. These two subtypes had distances between the No significant differences were observed regarding the origin of origin and the carotid bifurcation of 0.3 cm and 2.0 cm, respectively the lingual artery, neither by side nor by gender (p > 0.05). (Fig. 5). The mean distance between the independently originating lin- We have not observed statistically significant differences in the gual arteries and the carotid bifurcation was 1.32 cm with a distance of origin of the lingual artery, both in isolation and in the standard deviation of 0.76 cm. The range was established between form of the arterial trunk, neither by side nor by gender (p > 0.05). 0.1 and 4.1 cm. The caliber found for the lingual artery ranged from 0.1 cm to The mean distance between the origin of the linguofacial trunk 0.8 cm, with a mean caliber of 0.3 cm and a standard deviation of and the carotid bifurcation amounted to 1.39 cm with a standard 0.08 cm (Fig. 6). In the distribution of arterial caliber by side, we deviation of 0.82 cm and a range of 0.2–4.0 cm. In six body-donors have not observed statistically significant differences (p > 0.05). (2.9%; 6/207) the lingual artery originated from the bifurcation However, when evaluating gender differences, we have observed itself, of which five were in isolation and one in form of a linguofa- that the diameter of the lingual artery has been significantly greater cial trunk (Fig. 5). in men (p = 0.027). 3 R. Cobiella, S. Quinones, P. Aragones et al. Annals of Anatomy 238 (2021) 151789 Fig. 4. Isolated block of the carotid arteries to show two of the common patterns observed in this study. A. Left view of a thyrolingual trunk formed by the superior thyroid with the lingual artery. B. Left view of a linguofacial trunk constituted by the lingual and facial artery. CCa: common carotid artery, Ica: internal carotid artery, Eca: external carotid artery, TLT: thyrolingual trunk, St: superior thyroid artery, La: lingual artery, Fa: facial, Tlf: linguofacial trunk, Sla: superior laryngeal artery. Fig. 5. Frequency between the origin of the studied artery and the carotid bifurcation (distance in mm in the X-axis). Studied arteries: facial, occipital, ascending pharyngeal (I), ascending pharyngeal (II) and sternocleidomastoid artery. 3.2. Facial artery nated from the external carotid artery except for one that did so at the level of the carotid bifurcation. Therefore, the most fre- The facial artery was the largest artery that originates immedi- quent origin was the external carotid artery (99.03%; 205/207 [p ately cranial to the lingual artery. < 0.01]) either independently or in the form of an arterial trunk The artery was observed arising from three different levels, (Figs. 7 and 8). mainly from an independent branch originating isolated from The origin of the facial artery was investigated in a total of 77 the external carotid artery (171/207, 82.61%), as arterial trunks samples. Its origin was variable, being the most common with a (35/207, 16.9%) or isolated at the carotid bifurcation (1/207, 96.1% (74 cases) in the anterior face of the artery, the remaining 0.48%). In the case of the origin of the facial artery as an arte- three cases were in an antero-lateral, lateral, and postero-medial rial trunk (16.9%), it always arose together with the lingual artery position (1.3% each) (Fig. 3). except a unique thyrolinguofacial trunk. All these trunks origi- 4 R. Cobiella, S. Quinones, P. Aragones et al. Annals of Anatomy 238 (2021) 151789 Fig. 6. Frequency diameter in cm of the lingual, facial, occipital, ascending phayngeal and sternocleidomastoid artery. cm, centimeters. Fig. 7. Isolated block of left carotid arteries showing the variability of origin of different arteries. CCa: common carotid artery, Ica: internal carotid artery, Eca: external carotid artery, St: superior thyroid artery, La: lingual artery, Fa: facial, Oa: occipital artery. Ph: ascending pharyngeal artery. 5 R. Cobiella, S. Quinones, P. Aragones et al. Annals of Anatomy 238 (2021) 151789 Fig. 8. Isolated block of the carotid arteries showing the variability of origin of different arteries. A, C, left lateral views and B, D, right internal views. CCa: common carotid artery, Ica: internal carotid artery, Eca: external carotid artery, St: superior thyroid artery, La: lingual artery, Fa: facial, Oa: occipital artery. Ph: ascending pharyngeal. No statistically significant differences were observed regarding Table 1 Distances of the origin of the ascending pharyngeal artery regarding the occipital the origin of the facial artery with regards to the location, neither artery. by side nor by gender (p > 0.05). The distance between the origin of the facial artery and the Origin of the ascending pharyngeal artery. Total (n = 174) carotid bifurcation in the external carotid, in isolation, is shown (n = 23) cm in Fig. 5. N % The maximum distance at which the origin of the facial artery ≤0.5 14 60.9 Regarding the occipital 0.6−1 5 21.7 occurred, in the external carotid artery, was 4.5 cm of the carotid artery 1.1−1.5 1 4.3 bifurcation while the minimum was 0.2 cm away from the carotid 1.6−2 2 8.7 bifurcation. The mean was 2.08 cm with a standard deviation of 2.1−2.5 1 4.3 0.82 cm. N, sample size and cm, centimeters. The caliber of the facial artery was observed in 206 cases, 95 in male and 111 in female with results ranging from 0.2 cm to 0.8 cm. The mean value obtained was 0.36 cm with a standard deviation of The occipital artery’s origin was observed in 199 cases (90 in 0.23 cm (Fig. 6). men and 109 in female), finding values that ranged between 0.1 In the distribution of arterial caliber by side and gender we have cm and 0.9 cm. The overall mean diameter obtained was 0.27 cm not observed statistically significant differences (p > 0.05). with a standard deviation of 0.09 cm (Fig. 6). In the distribution of arterial caliber as well as origin by side and gender, we have not observed statistically significant differences (p > 0.05). 3.3. Occipital artery 3.4. Ascending pharyngeal artery The artery was observed arising from two different levels: exter- nal carotid artery (94.7%, 195/206) and carotid bifurcation (3.9%, It is the last of the great arteries described, classically located in 8/206, p < 0.01) (Figs. 7 and 8). Exceptionally, on the right side, the the carotid triangle and has the most variable origin of all collateral artery was not identified in three samples (1.4%, 3/206). branches (Figs. 7 and 8). Analyzing the origin of the occipital artery according to the side, The origin of the ascending pharyngeal artery was studied in there was a predominance of origin of the artery at the level of the 207 cases (95 men and 112 female), being observed at up to bifurcation on the right side (p = 0.033). eight different levels: external carotid (70.5%), occipital (13.5%), No statistically significant difference was observed regarding carotid bifurcation (9.7%), internal carotid (1.4%), common carotid gender (p > 0.05). artery (1%), facial (1%), lingual (0.5%) and superior laryngeal arter- Differing from the origin location of the upper mentioned lingual ies (0.5%); in 4 samples (1.9%), the ascending pharyngeal artery was and facial artery, the location of the origin of the occipital artery, in not identifiable. any of its levels, was the posterior face of the vascular axis in most In sum, the most frequent origin was observed at the level of the cases (74/85 87.1%). In the remaining cases, the origin was observed carotid arterial axis in 81.2% of the cases. No significant differences in a lateral position (4/85 4.7%), medial (4/85 4.7%), postero-medial were observed in the origin of the ascending pharyngeal artery nei- (2/85, 2.4%) and in a postero-lateral position (1/85, 1.2%, Fig. 3). ther by side nor by gender (p > 0.05). The distance of origin of the The distance from the origin of the occipital artery to the carotid ascending pharyngeal is shown in Table 1. bifurcation in the external carotid is shown in Fig. 5. In 8 sam- The ascending pharyngeal artery origin location was observed ples (3.9%; 8/203) the occipital artery originated at the level of the on the medial face of the vascular axis in most cases (60/70, 85.7%), carotid bifurcation itself. the remaining 10 cases were distributed as follows: posterior (5/70, The mean distance at which the origin was established was 1.8 7.1%), lateral (2/70, 2.9%), anterior (2/70, 2.9%) and, finally, postero- cm with a standard deviation of 1.15 cm and a range of 0.1–6.7 cm. medial (1/70, 1.5%) (Fig. 3). The distance from the origin of the 6 R. Cobiella, S. Quinones, P. Aragones et al. Annals of Anatomy 238 (2021) 151789 ascending pharyngeal artery to the carotid bifurcation in the arter- - Pattern III: The superior thyroid artery forms a common trunk ies that arise from the common and external carotid, is shown in with the lingual artery (thyrolingual trunk) while the facial artery Fig. 5. remains with an isolated origin. This pattern was observed in 2 In 13.5% of cases (28/207), the ascending pharyngeal artery arose of the 193 cases (1,04%). in a common trunk with the occipital artery. - Pattern IV: A common trunk formed by the superior thyroid, lin- The caliber of the ascending pharyngeal artery, measured in 198 gual and facial artery (thyrolinguofacial trunk). This pattern was cases (92 men, 106 female) showed a range of 0.05 cm to 0.3 cm. observed only in one case (0.52%). The overall mean diameter obtained was 0.17 cm with a standard deviation of 0.06 cm (Fig. 6). On the other hand, the distribution of the origins of the posterior We have not observed statistically significant differences for the arteries (occipital and ascending pharyngeal) raised four different distance of origin or the caliber of the ascending pharyngeal artery possibilities, being classified as types (these could appear on each neither as a function of the side nor as a function of gender (p > pattern): 0.05). - Type a: The posterior arteries originate independently. In our 3.5. Sternocleidomastoid artery study, this was the most frequent type (159/193, 82,4%). - Type b: The posterior arteries originate in a common trunk Despite the bibliography defined that there are actually two (27/193, 13.99%). sternocleidomastoid arteries, in the present study no distinction - Type c: The ascending pharyngeal artery is absent (4/193, 2.07%). was made between superior and inferior. Furthermore, only the - Type d: The occipital artery is absent (3/193, 1,55%). cases when its origin was located in the carotid axis have been studied (the rest were not considered). The total number of stern- To analyze if there are significant differences among authors ocleidomastoid arteries measured amounted to 43 cases (43/207, in the incidence of variations of the superior thyroid artery origins, 20.7%). 40 arteries originated at the level of the external carotid we have compared the observed data by means of the Fisher homo- artery (40/43; 93.02%), 2 cases (2/43, 4.7%) at the level of the carotid geneity test with a significance level alpha = 0.05. When comparing bifurcation and 1 case (1/43, 2.3%) at the level of the common authors with data obtained, results show that there are significant carotid artery. differences (p-value = 6.65e-06) when considering the four varia- The mean distance at which the origin was established, in the tion types. Anomalous larger percentages for pattern I and smaller external carotid artery, was 2 cm with a standard deviation of 1.11 for pattern II were reported by Ozgur et al. (2008), extremely larger cm and a range of 0.4–4.5 cm (Fig. 5). The only case originating at percentages por pattern III and anomalous smaller for pattern II the level of the common carotid was at 0.3 cm distance. were reported by Aaron and Chawaf (1967) and extremely large Most of the cases in which the sternocleidomastoid artery origi- for pattern IV by Zumre et al. (2005) and Adachi and Kihara (1928) nated from the external carotid artery did so in the territory where (Aaron and Chawaf, 1967; Adachi and Kihara, 1928; Ozgur et al., the occipital artery usually originated and not in the territory of the 2008; Zumre et al., 2005). The confidence interval for each varia- superior thyroid artery. tion type is given in Table 4. Fig. 10 shows the compared data within The mean diameter of the sternocleidomastoid artery amounted a box plot. to 0.13 with a standard deviation of 0.04 cm as well as a range of 0.05 cm to 0.3 cm (Fig. 6). 4. Discussion 3.6. Proposal of a new classification The course of the main branches of the external carotid artery is of great relevance for both diagnostic and therapeutic approaches. After the initial dissection, measuring procedure and statisti- The variability of these structures has been described several times, cal analysis, a thorough literature review with regard to currently but a large cohort was lacking a classification of defined variations available classification systems for the topography of the external and a categorization according to its prevalence. With the help of artery’s branches was performed. As a result, a new classification this study, which dealt with anatomical dissection as well as sta- system was developed dividing the collateral branches of the exter- tistical elaboration and literature research, this gap could be closed nal carotid artery into two groups: anterior branches (superior for the first time. thyroid, lingual and facial artery), and posterior branches (occip- ital and ascending pharyngeal artery), not including the superior 4.1. Lingual artery laryngeal artery and sternocleidomastoid due to their lower inci- dence. The most frequent origin of the lingual artery was the external The distribution of the anterior branches with regard to its dis- carotid artery (Adachi and Kihara, 1928; Hollinshead, 1954; Livini, tance from the carotid bifurcation was constant throughout the 1903a, b; Quain, 1844; Tubbs et al., 2016), being present in 95.7% entire sample: superior thyroid artery followed by lingual and facial of our study cohort. artery. The only observed variation, which maintains the previously In 19.18% of the cases, the origin of the lingual artery was joined mentioned sequence, was the association of the different branches by other branches, mainly the facial artery, forming a linguofa- in arterial trunks, either linguofacial (lingual and facial artery), or cial trunk, (17.62%), less frequently, the superior thyroid artery, thyrolingual (superior thyroid and lingual artery). thyrolingual trunk (1.04%), and exceptionally the thyrolinguofacial This fact determined 3 main patterns: (Fig. 9) trunk (0.52%). The percentage obtained in our series, although somewhat - Pattern I: the three anterior branches originate independently. It lower, is similar to that reported by previous literature (Adachi is the most frequent pattern, which was present in 80.83% 81.35% and Kihara, 1928; Hollinshead, 1954; Livini, 1903a, b; Quain, 1844; of our study cohort. Tubbs et al., 2016). On the contrary, our literature review found no - Pattern II: The superior thyroid artery arises separately, while study describing a bilateral linguofacial or thyrolingual trunk. How- the lingual and facial artery form a common trunk (linguofacial ever, in our sample, this bilaterality was observed in up to 27.8% of trunk). This type was observed in 17.62% of our study cohort. the linguofacial or thyrolingual trunk subtypes. The distance of the 7 R. Cobiella, S. Quinones, P. Aragones et al. Annals of Anatomy 238 (2021) 151789 Fig. 9. Drawing of the arterial patterns observed in this study. Four different patterns regarding the bifurcation of the anterior branches (superior thyroid, lingual and facial) and types of origin of the occipital and pharyngeal ascending arteries. TLT: thyrolingual trunk, LFT: linguofacial trunk, TLFT: thyrolinguofacial trunk, T: trunk La: lingual artery, st: superior thyroid artery, Fa: facial, oa: occipital artery, aph: ascending pharyngeal artery. 8 R. Cobiella, S. Quinones, P. Aragones et al. Annals of Anatomy 238 (2021) 151789 Table 2 Arrangement of the origin of the ascending pharyngeal artery in the carotid arterial axis and in the occipital artery. Comparison with the bibliography consulted. In the case of Livini (1903a,b) the percentage of cases of the internal carotid artery, carotid bifurcation, external carotid artery and absent cases (3%) amounted to 100% of the sample. n = sample size. Ascending pharyngeal Intern carotid Common carotid External carotid Carotid bifurcation Occipital Quain (1844) (n = 144) 6.2% – 73.6% 4.1% 13.2% Livini (1903a,b) (n = 200) 3% – 81% 10% 16.3% Adachi and Kihara (1928) (n = 128) 8% – 66% 26% Czerwinski (1981) (n = 240) – 2% 74% – 24% Our sample (2020) (n = 207) 1.4% 1% 70.5% 9.7% 13.5% Table 3 Situation of origin. Comparison of our results with those of Livini (1903a,b) if we analyze the terminology assigned for the different faces of the carotid arterial axis. Our sample (2020) Situation of origin Livini (1903a,b) Thyroid, lingual and facial Anterior Internal Thyroid, lingual and facial (30%) Ascending pharyngeal Medial Posterior Ascending pharyngeal and occipital Occipital Posterior External Occipital (30%) Lateral Anterior Facial Table 4 Arrangement of the anterior branches (superior thyroid, lingual and facial arteries), expressed in percentages. Authors Pattern I: Pattern II: Pattern III: Pattern IV: independently linguofacial thyrolingual thyrolinguofacial trunk trunk trunk Quain (1844) (n = 302) 79.3 20 0.7 0 Livini (1903a,b) (n = 200) 73.5 25 1.5 0 Adachi and Kihara (1928) (n = 300) 76.3 18.7 2 3 Aaron and Chawaf (1967) (n = 187) (anatomical) 73.2 20.9 5.9 0 Aaron and Chawaf (1967) (n = 100) (radiological) 65 26 9 0 Poisel and Golth (1974) (n = 156) 72.69 23.1 3.21 0.64 Czerwinski (1981) (n = 240) 80.9 17.5 1.6 0 Shintani et al. (1999) (n = 58) 65.5 31 3.5 0 Lucev et al. (2000) (n = 40) 80 20 0 0 Zumre et al. (2005) (n = 40) 75 20 2.5 2.5 Ozgur et al. (2008) (n = 40) 90 7.5 2.5 0 Sanjeev et al. (2010) (n = 37) 78.38 (29/37) 18.92 (7/37) 2.7 (1/37) 0 Mata et al. (2012) (n = 36) 77.8 19.4 2.8 0 Yonenaga et al. (2011) (n = 56) 69.6 28.6 1.8 0 Our study (2020) (n = 193) 80.82 17.62 (34/193) 1.04 (2/193) 0.52 (1/193) IC95% (p) [73.98;77.75] [19.16;22.74] [2;3.43] [0.15;0.74] Fig. 10. Box plot comparing authors. Results show that there are significant differences (p-value = 6.65e-06) when consider the four variation types. 9 R. Cobiella, S. Quinones, P. Aragones et al. Annals of Anatomy 238 (2021) 151789 linguofacial trunk origins was similar to the origin of the lingual and slightly covered by the angle of the mandible (Hollinshead, artery although more caudal to the usual facial artery’s origin. 1954), 2.5 cm from the carotid bifurcation (Livini, 1903a, b) and 0.5 From a surgical point of view, alterations in the course of the cm of the lingual artery (Tubbs et al., 2016). lingual artery are highly important, since the ligation of this artery The mean distance of the facial artery’s origin from the carotid depends on the identification of it in certain classical cervical tri- bifurcation was 2.08 cm, compared to 3.08 ± 1.18 cm as published angles (Pirogoff triangles, Lesser and Beclard) (Adachi and Kihara, by Yonenaga et al. (2011). 1928). In terms of arterial caliber, the differences of the results com- As for other authors, the origin at another level of the carotid pared to Czerwinski (1981) were more evident with 0.36 cm versus axis was very infrequent with seven cases at the level of the carotid 0.2 cm, respectively. No justification for such a wide difference, bifurcation mentioned as the lowest level by Livini (Livini, 1903a, b) up to 0.15 cm, was found; an artery that was always represented in three cases; two cases in the series by Adachi and Kihara (1928), with a caliber equal to or greater than that of the lingual artery one case in the series by Lucev et al. (2000), and one case described (Hollinshead, 1954; Janfaza, 2011; Tubbs et al., 2016). by Troupis et al. (2014) and four cases at the level of the common carotid artery (three cases in the series by Adachi and Kihara (1928) 4.3. Occipital artery and one case by Ambali and Jadhav (2012)). The lingual artery arises from the anterior (Hollinshead, 1954) In our series, the most frequent origin for the occipital artery was or internal (Tubbs et al., 2016) aspect of the external carotid artery, the external carotid artery, with 95% of the cases, which coincides above the superior thyroid artery. In our series the most frequent with the majority of previous studies (Adachi and Kihara, 1928; situation for the lingual artery was at the anterior level of the carotid Czerwinski, 1981; Hollinshead, 1954; Livini, 1903a, b; Quain, 1844; arterial axis with 76.6% of the cases. This is not consistent with the Tubbs et al., 2016). The percentage of cases (3.9%) originating at results from previous studies by Livini, where the medial origin was the level of the carotid bifurcation was higher than that observed shown to be the most common at 75% (Livini, 1903a, b). in literature with frequencies of 0.7% (Quain, 1844), 0.5% (Livini, Previously, the origin of the lingual artery was considered to be 1903a, b) and 0.3% (Adachi and Kihara, 1928). In most of our cases, at a distance of approximately 2 cm from the carotid bifurcation the origin at the carotid bifurcation was identified on the right side (Livini, 1903a, b; Tubbs et al., 2016) or 1 cm from the superior thy- (7 versus 1), obtaining a trend although no statistical significance roid artery, respectively (Tubbs et al., 2016). The measurements of has been reached (p = 0.06). our study show only congruent results concerning the distance to Also, in three cases (2.8%) no occipital artery was identified, this the superior thyroid artery at 0.85 cm. finding is similar to Livini’s series (1.5%) (Livini, 1903a, b). In the present study, the distance between the origin of the lin- As in our results, where in 88% of cases the occipital artery orig- gual artery at the external carotid artery and the carotid bifurcation inated at the posterior face of the carotid arterial axis, most of the ranged from 0.1 to 4.1 cm with a mean distance of 1.34 cm. These evaluated works in literature agree, establishing this surface as the results are similar to previous findings of Lucev et al. (2000) and most frequent (Hollinshead, 1954; Livini, 1903a, b; Tubbs et al., Lins et al. (2005) where the range was 0.5–3.7 cm and 0.5−4 cm, 2016). respectively. In our series, the mean distance from the carotid bifurcation was Concerning the superior thyroid artery, our mean diameter (0.32 1.8 cm, similar to previously published findings by Livini (Livini, cm) was slightly greater than that evaluated by Czerwinski (1981) 1903a, b) and Alvernia et al. (2006). These results are in accordance in his series, which was 0.28 cm. In this work, performing the anal- with previous findings reported in Livini’s series (Livini, 1903a, b), ysis in relation to side and gender, no significant differences were with a distance maximum of 6 cm in Livini’s series compared to observed in its origin, but in terms of arterial caliber, the diameter 6.7 cm in our result. However, Alvernia et al. differed radically with of the lingual artery was significantly greater in male (p = 0.027). both series, showing a range from 0.7 to 2.8 cm (Alvernia et al., 2006). 4.2. Facial artery As with the lingual artery, the mean diameter obtained in our results, 0.27 cm was clearly higher compared to results obtained The usual origin of the facial artery was located at the external by Czerwinski (1981) of 0.16 cm. carotid artery (Hollinshead, 1954; Livini, 1903a, b; Quain, 1844; With the exception of the difference observed in the origin of Tubbs et al., 2016) with a frequency of 99% in our study cohort. the occipital artery at the level of the bifurcation, which is more There were two cases originating at the level of the carotid bifur- prevalent on the right side (p = 0.06), no other differences, either cation, one isolated and another one in the form of a linguofacial as a function of side or gender, were found. trunk. Our literature review showed no similar variabilities; hence we firstly describe these two types of a facial artery origin. 4.4. Ascending pharyngeal artery It should be noted that the case of the lingual artery originating in the common carotid artery as well as the facial artery originat- The most common origin was the external carotid artery being ing at the level of the carotid bifurcation were observed at the same in our sample 70.5%. However, characteristically, it was a highly body-donor, on the left side. The superior thyroid artery arose 0.6 variable artery in terms of its origin, arising from other collat- cm below from the bifurcation, the lingual 0.3 cm below the bifurca- eral branches of the external carotid artery, especially the occipital tion too and the facial artery directly at the bifurcation. The occipital artery (Table 2). and the ascending pharyngeal arteries originated from the external In addition, two cases of an ascending pharyngeal artery orig- carotid at 0.1 cm and 0.6 cm above the bifurcation, respectively. inating from the facial artery have been found. This result is Classically, the origin of the facial artery was described with consistent with previously described cases in the literature (Adachi an anterior localization on the carotid vascular axis (Hollinshead, and Kihara, 1928; Tubbs et al., 2016). Exceptionally, one case orig- 1954; Tubbs et al., 2016). In the studies published by Livini (Livini, inating from the lingual artery and the other from the superior 1903a, b) the two most frequent origins were antero-internal with laryngeal artery previously described by Livini (Livini, 1903a, b). 70% and internal with 30%. In our series, in 96.1% of the cases, the The frequency distribution obtained in our results was compa- origin was established in an anterior face of the artery (Table 3). rable to previous literature, with the exception of cases that arose Classically, the origin of the facial artery was referred to in dif- from the internal carotid artery, in which a less percentage was ferent ways: at the level of the lower border of the digastric muscle found coinciding with Czerwinski (1981) (Table 2). 10 R. Cobiella, S. Quinones, P. Aragones et al. Annals of Anatomy 238 (2021) 151789 In four cases (1.9%) the pharyngeal ascending artery was not at 1.8 cm in 20% of cases. Very similar with the location that must identified, similar results were found in studies published by Quain be taken into account to avoid confusion of these two arteries. (1844) (one case, 0.7%) as well as Livini (Livini, 1903a, b) (six cases, 3%). Similar to the occipital artery, the ascending pharyngeal artery is defined as a posterior collateral branch of the external carotid artery 4.6. Arrangement and classification (Hollinshead, 1954; Tubbs et al., 2016). For Livini this situation was observed in up to 90% of his sample (Livini, 1903a, b). In our results, Looking at the anterior arterial branches studied in this cohort, in 85.7% of the cases the origin of the ascending pharyngeal artery 80.83% (156/193) of the superior thyroid, lingual and facial arteries was observed on the internal face of the carotid arterial axis. originated separately from the external or common carotid artery, We believe that it might be possible that in clinical practice there which is in accordance with previous studies (Adachi and Kihara, were no such marked discrepancies between our results and those 1928; Lucev et al., 2000; Mata et al., 2012; Ozgur et al., 2008; Poisel of Livini (Livini, 1903a, b) and that rather the difference is found in and Golth, 1974; Sanjeev et al., 2010; Shintani et al., 1999; Zumre the way in which the different faces of the carotid arterial axis have et al., 2005). Among the combined artery trunks, the linguofacial been cataloged, as represented in Table 3. trunk was always observed most frequently, except for the study Looking at it this way, there were practically no differences in conducted by Adachi hence a linguofacial trunk was not detected in the situation of origin as such, except for a discrepancy in the fre- his case series. In this study, the linguofacial trunk was observed in quency distribution of the facial and occipital artery. In these two 17.62% cases (34/193), while the previously reported linguofacial arterial branches, the congruence regarding the distribution fre- trunk frequency ranges from 7.5 to 31% (Lucev et al., 2000; Mata quency compared to the results by Livini is 30% (Livini, 1903a, b). et al., 2012; Ozgur et al., 2008; Poisel and Golth, 1974; Sanjeev et al., Regarding the distance of origin, the ascending pharyngeal 2010; Shintani et al., 1999; Zumre et al., 2005) (Table 4). artery is defined as the most variable collateral branch, which was The thyrolingual trunk was reported by other authors with a described in various locations including the artery being close to prevalence ranging from 2.5 to 3.5% (Mata et al., 2012; Ozgur et al., the carotid bifurcation (Hollinshead, 1954; Janfaza, 2011) or at the 2008; Poisel and Golth, 1974; Sanjeev et al., 2010; Shintani et al., same height as the lingual artery, at 2 cm distance to the carotid 1999; Zumre et al., 2005), while the prevalence observed in the bifurcation (Livini, 1903a, b; Tubbs et al., 2016). present study was 1.4%. (2/193) (Table 4). Only one thyrolinguofa- The mean arterial caliber of the ascending pharyngeal artery cial trunk was found (0.52%), a very rare variation, evaluated in our was 0.17 cm, and therefore, if we eliminate occasional collateral previous article (Vazquez et al., 2009); other authors reported a fre- branches of the carotid arterial axis (sternocleidomastoid arteries), quency up to 3% (Adachi and Kihara, 1928; Mata et al., 2012; Ozgur it was the branch with the smallest caliber of the group studied. et al., 2008; Poisel and Golth, 1974; Sanjeev et al., 2010; Shintani In the literature consulted, we did not find any previous studies et al., 1999; Zumre et al., 2005) (Table 4). reporting on the arterial diameter of the ascending pharyngeal To our knowledge, from the previous literature reviewed, only artery. two authors, Livini and Aaron, performed classifications of arterial Given the great variability regarding the origin of the ascending patterns in the branches of the external carotid artery (Aaron and pharyngeal artery, which was highlighted previously, it should be Chawaf, 1967; Livini, 1903a, b). Based on the established classifi- noted that from a surgical point of view the identification of this cation system, this study intended to obtain similar patterns, from artery is not predictable based on its origin. Alternatively, the iden- which comparisons could be made. tification of the ascending pharyngeal artery should be provided The studies by Livini (Livini, 1903a, b) consists of an exposi- using the location and the caliber; that is, a small-caliber artery tion of the different combinations of arterial branches, which were located on the inner side of the carotid arterial axis. The high vari- observed in the study cohort although no distribution frequency ability of 18.8% in the origin of this artery should be noted with was shown, which limits the applicability of the classification for regards to its identification, especially because of the clinical rel- daily clinical work. evance, such as during an intraoperative ligation. Tumor lesions Aaron and Chawaf (1967) developed another classification, located in the pharynx or at the skull base, such as glomus tym- using the distance of the origin as a variable. However, in our results, panicum and jugulare or nasopharyngeal angiofibroma, may be this character was the most variable and the one with the most dis- mainly supplied by this artery (Lins et al., 2005), whose treatment persion, hence, this parameter is neither applicable for a sufficient may be a surgical approach, if a “watch and wait” option or other usability. approaches, such as endovascular embolization or radiosurgery is In our case, the arterial patterns were developed based on the not applicable. origin of the collateral branches emitted by the carotid arterial axis at the upper carotid triangle level, allowing a new point of view compared with these previous classifications. These results pro- 4.5. Sternocleidomastoid artery vide clearer guidelines for orientation against possible variations compared with the classical pattern. All authors recognized that there are two different sternoclei- Therefore, a thorough understanding of the branches of the ECA domastoid arteries, superior and inferior (Hollinshead, 1954). The might lead to significant benefits in new techniques, e.g., exter- superior sternocleidomastoid artery arose from the occipital artery nal carotid and internal carotid (EC-IC) minimally invasive surgery and the inferior from the superior thyroid artery (Hollinshead, (Fischer et al., 2016) or new intervention methods for chronic sub- 1954), however, a direct origin from the external carotid artery was dural hematoma via embolization of branches of the ECA (Al-Mufti reported in 42% of cases or 37% of cases, respectively (Livini, 1903a, et al., 2021). The absence of a thyrolinguofacial trunk in our sam- b). Our results only show an origin from the external carotid artery ples, being a very rare variation, should be mentioned here again in 19.3%. Moreover, our result show origins arising from the carotid due to the fact that, although a rarity, it should be kept in mind for bifurcation (2/43, 4.65%) and one from the CCA (1/43, 2.33%), these safe interventional procedures (Vazquez et al., 2009). Furthermore, cases we did not find in the literature consulted. the anatomy and classification of the different branches, especially In the same way we did not find any reference to the distance facial artery, lingual artery, ascending pharyngeal artery are of high of the superior sternocleidomastoid artery from the carotid bifur- relevance for ENT approaches and surgeries or reconstruction plas- cation, that in our results was of 2 cm meanwhile the occipital was tic surgeries. 11 R. Cobiella, S. Quinones, P. Aragones et al. Annals of Anatomy 238 (2021) 151789 5. Conclusions improve patient care. Therefore, again, these donors and their fam- ilies deserve our highest gratitude (Iwanaga et al., 2021). All the different variables studied as the origin and calibers of the main collateral arteries of the external carotid (lingual, facial, References occipital, ascending pharyngeal and sternocleidomastoid arteries) have a substantiable importance in daily clinical practice due to Aaron, C., Chawaf, A., 1967. Variations de la carotide externe et de ses branches. Bull. Assoc. Anat. 13, 125–133. growing applications e.g., in Interventional Radiology techniques. Adachi, B., Kihara, T., 1928. Das Arteriensystem der Japaner. Verlag der Kaiserlich- The new classification proposed could allow a more precise knowl- Japanischen Universitat, zu Kyoto, pp. 26–46, Kommission bei Maruzen Co. edge and control of these anatomical variations, aiming to support Al-Mufti, F., Kaur, G., Amuluru, K., Cooper, J., Dakay, K., El-Ghanem, M., Pisapia, J., Muh, C., Tyagi, R., Bowers, C., 2021. Middle meningeal artery embolization using clinicians in the interpretation of imaging modalities. combined particle embolization and n-BCA with the dextrose 5% in water push technique for chronic subdural hematomas: a prospective safety and feasibility study. Am. J. Neuroradiol. 42, 916–920. Author contribution Alvernia, J.E., Fraser, K., Lanzino, G., 2006. The occipital artery: amicroanatomical study. Oper. Neurosurg. 58, ONS–114-ONS-122. Cobiella R: Project development, data collection, Manuscript Ambali, M., Jadhav, S., 2012. Variations in bifurcation point and branching pattern of common carotid arteries: a cadaveric study. J. Pharm. Biomed. Sci. 25, 147–151. writing. Czerwinski, F., 1981. Variability of the course of external carotid artery and its rami Quinones S: Data analysis, Manuscript writing, Manuscript edit- in man in the light of anatomical and radiological studies. Folia Morphol. (Warsz) ing. 40, 449–453. Fischer, G., Senger, S., Sharif, S., Oertel, J., 2016. Superficial temporal artery to mid- Aragones P: Manuscript writing, Manuscript editing. dle cerebral artery bypass via a minimized approach: operative nuances and León X: Data analysis. problem-solving aspects. World Neurosurg. 88, 97–103. Abramovic A: Data collection, Data analysis, Manuscript editing. Germans, M.R., Regli, L., 2014. Posterior auricular artery as an alternative Vazquez T: Data collection, Data analysis, Manuscript editing. donor vessel for extracranial-intracranial bypass surgery. Acta Neurochir. 156, 2095–2101. Sanudo J: Data collection, Data analysis, Manuscript writing, Gluncic, V., Petanjek, Z., Marusic, A., Gluncic, I., 2001. High bifurcation of common Manuscript editing, Supervision. carotid artery, anomalous origin of ascending pharyngeal artery and anomalous Maranillo E: Data collection, Data analysis, Manuscript writing, branching pattern of external carotid artery. Surg. Radiol. Anat. 23, 123–125. Hollinshead, W.H., 1954. Anatomy for Surgeon. Cassell. Manuscript editing. Iwanaga, J., Singh, V., Ohtsuka, A., Hwang, Y., Kim, H.J., Moryś, J., Ravi, K.S., Ribatti, Olewnik L: Data analysis, Manuscript editing. D., Trainor, P.A., Sañudo, J.R., 2021. Acknowledging the use of human cadaveric Simon de Blas C: Data analysis, Manuscript editing. tissues in research papers: recommendations from anatomical journal editors. Clin. Anat. 34, 2–4. Parkin Ian: Project development, data collection. Janfaza, P., 2011. Surgical Anatomy of the Head and Neck. Harvard University Press. Konschake M: Data analysis, Manuscript writing, Manuscript Konschake, M., Brenner, E., 2014. “Mors auxilium vitae”—causes of death of body editing, Supervision. donors in an Austrian anatomical department. Ann. Anat. 196, 387–393. Lins, C.C.S.A., C.J, Nascimento, D.L.D., 2005. Extraoral ligature of lingual artery: anatomic and topographic study. Int. J. Morphol. 23, 271–274. Ethical approval details Livini, F., 1903a. L’arteria carotis externa. Richerche Arch. Ital. Anat. Embriol. 2, 653–741. Livini, F., 1903b. The type and normal variations della carotis externa. Arch. Ital. Biol. The individuals had given their written informed consent for 39, 487. their use for scientific purpose prior to death. According to National Lucev, N., Bobinac, D., Maric, I., Drescik, I., 2000. Variations of the great arteries in the carotid triangle. Otolaryngol. Head. Neck Surg. 122, 590–591. Law, scientific institutions (in general Institutes, Departments or Mata, J.R., Mata, F.R., Souza, M.C., Nishijo, H., Ferreira, T.A., 2012. Arrangement and Divisions of Medical Universities) are entitled to receive the body prevalence of branches in the external carotid artery in humans. Ital. J. Anat. after death mainly by means of a specific legacy, which is a special Embryol. 117, 65–74. Ozgur, Z., Govsa, F., Ozgur, T., 2008. Anatomic evaluation of the carotid artery bifur- form of last will and testament. No bequests are accepted without cation in cadavers: implications for open and endovascular therapy. Surg. Radiol. the donor having registered their legacy and been given appropriate Anat. 30, 475–480. information upon which to make a decision based upon written Poisel, S., Golth, D., 1974. Variability of large arteries in the carotid trigone. Wien. informed consent (policy of ethics); therefore, an ethics committee Med. Wochenschr. (1946) 124, 229–232. Quain, R., 1844. The Anatomy of the Arteries of the Human Body: and Its Applica- approval was not necessary (Konschake and Brenner, 2014). tions to Pathology and Operative Surgery with a Series of Lithographic Drawings. Taylor and Walton. Rajamani, K., Chaturvedi, S., 2011. Stroke prevention—surgical and interventional Consent to publish approaches to carotid stenosis. Neurotherapeutics 8, 503–514. Sanjeev, I., Anita, H., Ashwini, M., Mahesh, U., Rairam, G., 2010. Branching pattern of Not applicable. external carotid artery in human cadavers. J. Clin. Diagn. Res. 4, 3128–3133. Shintani, S., Terakado, N., Alcalde, R.E., Tomizawa, K., Nakayama, S., Ueyama, Y., Ichikawa, H., Sugimoto, T., Matsumura, T., 1999. An anatomical study of the arter- ies for intraarterial chemotherapy of head and neck cancer. Int. J. Clin. Oncol. 4, Funding sources 327–330. Troupis, T., Michalinos, A., Dimovelis, I., Demesticha, T., Vlasis, K., Skandalakis, P., This research did not receive any specific grant from funding 2014. Bilateral abnormal origin of the anterior branches of the external carotid agencies in the public, commercial, or not-for-profit sectors. artery. Ann. Vasc. Surg. 28, 494.e5–494.e7. Tubbs, R.S., Shoja, M.M., Loukas, M., 2016. Bergman’s Comprehensive Encyclopedia of Human Anatomic Variation. John Wiley & Sons. Vazquez, T., Cobiella, R., Maranillo, E., Valderrama, F.J., McHanwell, S., Parkin, I., Conflict of interest Sanudo, J.R., 2009. Anatomical variations of the superior thyroid and superior laryngeal arteries. Head Neck 31, 1078–1085. All authors have nothing to declare. No outside funding was Yonenaga, K., Tohnai, I., Mitsudo, K., Mori, Y., Saijo, H., Iwai, T., Yonehara, received. Y., Ota, Y., Torigoe, K., Takato, T., 2011. Anatomical study of the external carotid artery and its branches for administration of superselective intra- arterial chemotherapy via the superficial temporal artery. Int. J. Clin. Oncol. 16, 654–659. Acknowledgements Zumre, O., Salbacak, A., Cicekcibasi, A.E., Tuncer, I., Seker, M., 2005. Investiga- tion of the bifurcation level of the common carotid artery and variations of The authors wish to express their sincere gratitude to the the branches of the external carotid artery in human fetuses. Ann. Anat. 187, anatomical body-donors, who bequeathed their bodies for medical 361–369. education and basic science research. Results from such research can potentially increase mankind’s overall knowledge that can then 12