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Introduction
The infrahyoid muscles, which include the sternohyoid, sternothyroid, thyrohyoid, and omohyoid, play a crucial role in moving and stabilizing the larynx and hyoid bone, both of which are essential for swallowing and speech [1]. These muscles are innervated by the ansa cervicalis, except for the thyrohyoid muscle, which is innervated by a separate branch of the anterior ramus of spinal nerve C1 [1, 2]. Infrahyoid innervation pattern has historically been a subject of interest due to the discrepancies in its connection with the hypoglossal [1-3].
The infrahyoid muscles are enclosed by the superficial muscular layer of the pretracheal fascia of the neck, that envelops the neck viscera. This unique anatomical phenomenon of visceral fascia surrounding striated muscles may be explained by Henry Gray’s theory of the common embryological origin and shared innervation of the infrahyoid muscles with the diaphragm and the heart. The infrahyoid muscles and the diaphragm, together with the intrinsic muscles of the tongue, arise from a continuous premuscle mass extending from the tongue to the lateral neck region. This early structure is initially connected to the hypoglossal nerve and branches of the upper cervical nerves. During development, the mass divides, with the portions forming the infrahyoid muscles and diaphragm being separated by the developing heart. As the heart descends into the thorax, the diaphragmatic portion of the mass is drawn down into the thoracic cavity along with its nerve supply, while the infrahyoid muscles converge toward the midline of the neck [4, 5].
Despite their small size, the infrahyoid muscles are clinically significant due to their role in neck surgeries and cancer staging. Variations in these muscles and the ansa cervicalis are often underreported and insufficiently documented in the literature, which can negatively impact surgical planning and interventions, potentially affecting procedural success and patient outcomes.
This article aims to address this gap by providing a comprehensive systematic review of the anatomical variations of the infrahyoid muscles and the ansa cervicalis and proposing a new classification system for the many consistency and morphometric variations of the omohyoid muscle.
Review
Methods
A comprehensive search of the PubMed and Google Scholar databases was conducted up to September 19, 2024, using the keywords ‘infrahyoid muscles AND variation,’ ‘omohyoid muscle AND variation,’ ‘sternohyoid muscle AND variation,’ ‘sternothyroid muscle AND variation,’ ‘thyrohyoid muscle AND variation,’ ‘ansa cervicalis AND variation,’ and ‘strap muscles AND variation.’ The study was restricted to English-language, human-based articles. An additional search for the relevant studies cited in the references of the reviewed articles was also performed.
The search, adopting the evidence-based principles in anatomy, aimed to identify morphometric and consistency anatomical variations [6]. Eligibility was assessed using the PICOTS framework (Supplementary Table 1). In detail, articles were excluded if they were duplicates, lacked full text, or only mentioned infrahyoid muscles in the title or abstract without providing substantive information on their variations or innervation in the main text. We also excluded studies describing new neck muscles that did not share the same origin or insertion as the infrahyoid muscles. Regarding the ansa cervicalis, we included articles that specifically addressed absence or abnormalities in the formation of the ansa cervicalis, or of the inferior or superior roots, in order to examine any potential relationship with infrahyoid muscle variations; therefore, variations in the ansa cervicalis branching pattern or location were excluded.
For every included study, data concerning the surname of the first author, the year of publication, the number of cases reported, the variants concerning the omohyoid, the sternohyoid, the sternothyroid, the thyrohyoid, and any new type of infrahyoid muscle, as well as the ansa cervicalis were concentrated in a Microsoft Excel spreadsheet (Microsoft).
The anatomical quality assessment (AQUA) tool was employed to further evaluate the quality of the extracted records. This tool is designed to assess the risk of bias in anatomical studies across five domains: objectives and subject characterization, study design, methodology characterization, descriptive anatomy, and reporting of results. In each domain, questions are answered with ‘yes’, ‘no’, or ‘unclear’. If all questions within a domain are answered with ‘yes’, the risk of bias for that domain is considered low. A response of ‘no’ or ‘unclear’ indicates a high risk of bias in that domain. Studies were classified as having a high risk of bias if 4 or 5 domains were rated as high risk, moderate risk if 2 or 3 domains were rated high risk, and low risk if 0–1 domain was rated high risk. Only articles with a low or moderate risk of bias were included in this study. The quality assessment of the included studies is presented in Supplementary Tables 2 and 3 [7].
All steps including literature search, study selection, data extraction, and quality assessment were independently carried out by two researchers (NM, and VP). The third author (AF) was responsible for cross-checking in case of discordance. The study has been registered at the PROSPERO database on September 17, 2024 (Study ID: CRD42024591744).
Terminology
Due to the potentially confusing terms coined by the authors to the infrahyoid muscles’ variations, we followed the consistent anatomical terminology, as detailed below:
-‘Absent’ referred to a missing muscle.
-‘Accessory muscle’ applied to any muscle that appeared alongside the main muscle, sharing the same origin, insertion, or both.
-‘Abnormal origin’ referred to muscles that originated from a different point than the typically described.
-‘Abnormal insertion’ referred to muscles with an insertion point different than the typically described. The subtype ‘atypical’ was included for cases where the abnormal insertion was extraordinary and reported in a unique study.
-‘Abnormal course’ was used for muscles whose course deviated from the norm.
-‘One-belly’ referred to muscles missing the intermediate tendon or one of their bellies.
-‘Tendinous belly’ described a muscle belly that was replaced by a tendon.
-‘Additional belly’ described the presence of a supernumerary belly; multiple muscle heads were classified as additional bellies.
-‘Azygos’ referred to muscles originating on one side of the body and crossing to the opposite side. The reported right or left side relates to the side of origin.
-‘Slip’ was used for a small bundle of muscle fibers with a different course, origin, or insertion.
Finally, we adopted the names of the atypical infrahyoid muscles, as they were suggested by the authors. Any unnamed muscle of the anterior neck, that did not pertain to any known infrahyoid muscles, was classified as an atypical muscle, termed as “accessory infrahyoid muscle.”
Results
We included 84 records from 77 studies that documented variations in the infrahyoid muscles, the ansa cervicalis, or both (Fig. 1) [8]. Supplementary Table 4 provides a summary of these findings [9-41].
Omohyoid variation
We classified omohyoid muscle variations into two primary groups. The consistency variations are used to describe numerical variations in the infrahyoid muscles, referring to the absence of a muscle or the presence of an additional muscle or belly. These variations comprise four types, indicated by Roman numerals: Type I, absent muscle; Type II, absent intermediate tendon (one-belly); Type III, additional belly; and Type IV, accessory muscle. Morphometric variations encompass abnormalities in the muscle’s origin, insertion, or course, along with the presence of atrophy, organized into four categories and indicated by English capital letters Type A, abnormal origin (clavicular); Type B, abnormal insertion with 3 subtypes: (1) additional insertion into sternohyoid, (2) only insertion into sternohyoid, and (3) atypical; Type C, abnormal course (posterior to the internal jugular vein); and Type D, tendinous (superior) belly. When both consistency and morphometric variations were present, both classification systems were applied.
Table 1 maps the reviewed studies of omohyoid variations to their corresponding consistency and morphometric categories, or their combinations, except for the consistency variation IV of the accessory omohyoid muscle, which is specifically detailed in Table 2 [42-80]. The morphometric classification system used for the main omohyoid was also applied to the accessory omohyoid muscle, indicating that both share a similar pattern of morphologic variations.
We propose the following nomenclature for each omohyoid muscle variation: each variation is denoted as N/N, where the first letter represents the consistency variation (Fig. 2) and the second represents the morphometric variation (Fig. 3). Specifically, for the consistency variation of the accessory omohyoid muscle, we recommend using a lowercase letter to denote the morphometric component (e.g., IV/n) (Fig. 4). Only variations that were reported with high incidence are depicted in the Figs. 2–4.
Sole consistency variations of the omohyoid muscle are more common than sole morphometric variations (23/17). The abnormal clavicular origin and the tendinous superior belly were the most common morphometric variations, while the accessory omohyoid was the most frequently observed consistency variation (Fig. 5). The abnormal course of the omohyoid muscle was consistently noted to pass behind the internal jugular vein and observed exclusively on the left side. Omohyoid variation involving an additional belly was found only on the right side. The omohyoid muscle was the only infrahyoid muscle to exhibit bilateral variations. A case of an absent omohyoid muscle without an accessory muscle, as well as a case of a one-belly omohyoid muscle with a clavicular origin, was found bilaterally in the main omohyoid muscle. No records exist of the omohyoid muscle exhibiting an azygos variant.
Accessory omohyoid muscles were identified in 20 cases, with a higher prevalence on the right side compared to the left (12/8). The three bilateral cases of the accessory omohyoid muscle exhibited clavicular origin (Fig. 6). The subtype of atypical insertion was observed exclusively in conjunction with clavicular origin. Notably, none of the accessory muscles exhibited an intermediate tendon.
Sternohyoid variation
In one case, the sternohyoid muscle was absent on the right side, while in two cases an accessory sternohyoid and an azygos accessory sternohyoid were observed, both on the left side.
Sternothyroid variation
The sternothyroid muscle was reported absent in one case, with an abnormal insertion in another, and having two additional slips in a third case. An azygos accessory sternothyroid muscle was also observed. Interestingly, all sternothyroid variations occurred on the right side.
Thyrohyoid variation
The only documented variation of the thyrohyoid muscle was the presence of two heads on the left side, with no reports of an accessory thyrohyoid muscle, making it the only infrahyoid muscle without an accessory variation and the more anatomically constant of the four.
Atypical infrahyoid muscle variation
The levator glandulae thyroideae is the most common atypical form of infrahyoid muscles, since it had been documented in 9 of the 11 reported cases, with 4 on the right side and 5 on the left side.
There are only two other single cases of atypical infrahyoid muscles. The first muscle, on the left side, originated from the manubrium and the adjacent region of the clavicle and crossed deep to the posterior bellies of the digastric and stylohyoid muscles before bifurcating into a Y-shape. The second muscle, on the right side, originated from the manubrium and inserted into the clavicle, after looping around the intermediate tendon of the omohyoid muscle.
Ansa cervicalis variation
We documented 29 cases of ansa cervicalis variations (Fig. 7), involving either the loop or the superior and inferior roots. The most frequent variation of the ansa cervicalis involved the superior root, where it ran with the vagus nerve instead of the hypoglossal nerve. In cases of absent ansa cervicalis, it was more often replaced by the vagocervical complex. The most common variation of the inferior root was its complete absence. Three cases of bilateral variations included an abnormal superior root accompanying the vagus nerve, the replacement of the ansa cervicalis by a vagocervical complex, and the duplication of the inferior root. Only one paper reported ansa cervicalis variations combined with omohyoid variation, so it is pointless to examine any correlation of the two.
Discussion
Omohyoid muscle variations constituted half of our examined cases. Omohyoid variability was significant, compared to the other infrahyoid muscles, potentially reflects different evolutionary mechanisms. The omohyoid and sternohyoid muscles are typically described constituting the superficial layer of infrahyoid muscles, but only the omohyoid is embryologically part of that layer. This differentiation occurs between 54 and 59 days of gestation; by embryonic day 54, the approximation of the infrahyoid muscle masses is nearly complete, allowing for a clearer distinction among the sternohyoid, sternothyroid, thyrohyoid, and omohyoid muscles. In the next 5 embryonic days, the omohyoid muscle extends dorsally to reach the scapula, and by this point, the muscles have nearly attained their adult form. This theory may account for the multiplicity of the variations of the omohyoid muscle [5].
In 1960, Yamada was the first to introduce a classification system for omohyoid muscle variations, identifying six distinct types [66]. Yamada’s classification overlooked variations involving atypical courses, tendinous bellies, or connections between the omohyoid and other muscles [42-46]. It also failed to incorporate earlier descriptions of atypical omohyoid muscle [81].
Many years later, in 2006, Sukekawa and Itoh [82] investigated the abnormalities of the superior belly of the omohyoid muscle, classifying cases with abnormal insertion into both the hyoid bone and the sternohyoid muscle. However, their classification did not include other omohyoid muscle variants, as described by, Taylor [81], and Tubbs et al. [47], despite these being among the earliest documented omohyoid muscle variants in the literature.
The term ‘cleidohyoid’, meaning a muscle coursing from the clavicle to the hyoid bone, has been inconsistently applied and misinterpreted in the literature. Several studies used this term to describe the abnormal origin of the omohyoid muscle from the clavicle, contrasting with other studies reporting as cleidohyoid the abnormal origin of an additional muscle, while the main omohyoid muscle was normally present [48-52, 69-77].
Loth [83] presented a classification for the “cleidohyoid muscle”, which overlooked the cases where the cleidohyoid is an accessory muscle, since it coexists with the typical omohyoid. It also failed to include instances where the cleidohyoid inserted into the omohyoid and fused with its tendon [67, 68]. Bergman et al. [3] suggested that the absence of the omohyoid’s inferior belly explains the superior belly’s origin from the clavicle and gives rise to the cleidohyoid muscle. However, our findings reveal that the presence of the cleidohyoid with an intact intermediate tendon, and therefore two bellies, is a common variation. This indicates that the clavicular origin of the omohyoid does not necessarily imply the absence of its inferior belly.
Due to this overlapping terminology, we avoided using the term cleidohyoid. To address the anatomical misperceptions, we assumed that this term applies for any muscle originating from the clavicle and inserting into the hyoid bone, with or without an intermediate tendon, and classified it as a morphometric variation (clavicle origin) of the main omohyoid or the accessory omohyoid muscle.
We introduce a refined classification of omohyoid muscle variations, incorporating all cases reported in the literature and accounting for both consistency and morphometric differences. This updated system may prove valuable for anatomists and clinicians, as earlier classifications are incomplete due to their omission of some variants. The limited reports on the sternohyoid, sternothyroid, and thyrohyoid muscles’ variations result in the lack of related classifications.
Despite their small size, the infrahyoid muscles and their innervation are crucial in clinical practice, especially in neck surgeries. The omohyoid muscle is a key landmark for identifying level III and IV lymph node metastases [1]. Accurate cancer staging relies on locating lymph node involvement, and any variation in the omohyoid muscle can affect the identification of surrounding structures. Thus, developing a comprehensive classification of omohyoid variations is vital for improving clinical outcomes.
The sternohyoid and sternothyroid muscles require careful management to ensure optimal access to the thyroid gland in thyroidectomy [84]. Nayak et al. [85] noted that an abnormal sternohyoid course can complicate surgery, underscoring the importance of surgeons’ awareness of such variations. The levator glandulae thyroideae muscle was first studied for its frequency by Lehr in 1979 [86], is a common anatomical variant, that often appears alone or alongside other infrahyoid variations. Due to its proximity to the thyroid, knowledge of this muscle possible presence prevents confusion with other neck structures during surgery [87]. Mori’s [88] classification of the levator glandulae thyroideae covers most cases, though Loukas et al. [89] described a unique variation with three distinct muscle slips.
Infrahyoid muscles are also essential in head and neck reconstruction surgeries. According to Di Maio et al. [90], infrahyoid myocutaneous flaps have a necrosis or fistula rate of less than 10%, when used in reconstructive surgery for oral cavity and laryngopharynx defects. The flap’s anatomical location allows the surgeon to perform both tumor removal and reconstruction without patient repositioning, unlike flaps from other areas that may also require a different specialist [90]. The widespread use and low complication rates of infrahyoid muscles make them ideal flaps, on the condition that surgeons acknowledge their variations.
The only combined variation of the infrahyoid muscles and of the ansa cervicalis, described by Sonne, involves the fusion of the omohyoid with the sternocleidomastoid muscle, and the ansa cervicalis replacement by a complex of the vagus and the accessory nerve [46]. This report suggests that the muscles’ anatomical variations are not necessarily associated with variations in their innervation. The lack of correlation between infrahyoid muscle variations and the ansa cervicalis anomalies may be the result of underreporting in medical literature, since most of the reports on infrahyoid muscles’ variations omitted to search for coexisting variations in the ansa cervicalis.
The ansa cervicalis complex innervates three of the four infrahyoid muscles and it is formed by two roots from the anterior rami of the first three or four cervical spinal nerves. It is classified into three types—medial, lateral, or mixed—based on its relationship to the internal jugular vein [1, 2]. Jelev [91] proposed a classification of the variations in the superior and inferior roots, noting that the superior root may run alongside the vagus nerve, forming an atypical ansa cervicalis. Interestingly, this configuration (the superior root running with the vagus nerve) was the most frequent variation of the ansa cervicalis in our study. We documented three cases of the ‘vagocervical complex’, a variation not reported by Jelev [91], in which the cervical nerves connect directly to the vagus nerve, compensating for the absence of the ansa cervicalis. These findings highlight the role of the vagus nerve in transmitting cervical nerve fibers to the infrahyoid muscles when the ansa is abnormal or absent. They also reaffirm the 1955 revision by the Paris Nomina Anatomica, which replaced the term ‘ansa hypoglossi’ with ‘ansa cervicalis,’ a terminology shift that has remained in use ever since [92].
Three studies have investigated the use of the ansa cervicalis or its branches in the innervation of the recurrent laryngeal nerve, which was first described by Frazier [93]. Fadhil et al. [94] in their systematic review investigated the ideal timing for the reinnervation by the ansa cervicalis after recurrent laryngeal injury. Several studies have examined the position of the ansa cervicalis and its relationship with the internal jugular vein, which is particularly relevant for its use in surgical reinnervation procedures, as highlighted in the review by Loukas et al. [95] and the classification approach by Shvedavchenko et al. [96]. However, our study did not address positional variations of the ansa cervicalis, as we focused specifically on variations in ansa cervicalis formation correlated with the infrahyoid muscles. Kent et al. [97] reported a novel application of the ansa cervicalis, combining stimulation of its branch for the sternothyroid muscle with hypoglossal nerve stimulation to alleviate symptoms of obstructive sleep apnea. In a clinical trial, Li et al. [98] proposed that bilateral stimulation of the ansa cervicalis produced more significant effects in reducing collapse of the palate, oropharyngeal lateral walls, and epiglottis. Despite the significant applications of the ansa cervicalis, there is a notable lack of detailed descriptions regarding the functional consequences of its injury or severance, that is a common occurrence, as highlighted by Accord et al. [99], in carotid endarterectomy.
Despite their clinical applications, ansa cervicalis and infrahyoid muscles are often sacrificed during surgery with minimal or no apparent consequences, raising questions about their true function and clinical significance [90, 94, 100]. This highlights the need to re-evaluate the functional role of the infrahyoid muscles. Further investigation is warranted to clarify these aspects.
Conclusion
Anatomical literature continues to get enriched with new variations, crucial for advancing clinical knowledge. This review specifically address the infrahyoid muscles variations and develops a comprehensive new classification system for the omohyoid muscle, filling important gaps in existing classification systems and highlighting the need for an updated framework. These variations are important due to the infrahyoid muscles’ involvement in neck surgical procedures, including cancer staging, reconstruction and thyroid surgery, where even minor deviations can affect clinical outcomes. Interestingly, they are not accompanied by the ansa cervicalis variations, which may play a significant role during the repair of recurrent laryngeal nerve injuries and the treatment of obstructive sleep apnea.
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