Abstract
Objective:
To investigate the diagnostic value of the Yin-Yang tongue sign in patients with tongue deviation.
Methods:
According to the presence of the Yin-Yang tongue sign on CT/MR, 107 patients with tongue deviation were divided into a positive group and a negative group. The involvement categories of the hypoglossal canal (HC) in the positive group were evaluated and classified as HC dilation and HC erosion. The correlations between HC involvement categories and the presence of the sign were analysed.
Results:
There were 55 cases (55/107, 51.4%) in the positive group and 52 cases (52/107, 48.6%) in the negative group. Hypoglossal nerve (HN) involvement mainly occurred in the skull base (61.8%), skull base and carotid space (10.9%), and carotid space segment (12.7%). Neurogenic (50.9%), squamous cell carcinoma (14.5%), and metastases (12.7%) were the predominant aetiologies. The sensitivity, specificity, and accuracy of this sign for suggesting skull base lesions around HC were 72.4%, 80.8%, and 76.6%, respectively. In the positive group, HC dilation was seen in 21 patients (21/55, 38.2%) and 21 cases were all benign. HC erosion were noted in 19 patients (19/55, 34.5%), of whom 12 cases were malignant.
Conclusion:
The Yin-Yang tongue sign is formed by unilateral tongue atrophy and fat infiltration caused by lesions in the HN pathway, especially compressive or invasive lesions involving the skull base segment.
Keywords: Hypoglossal nerve, Hypoglossal nerve palsy, Hypoglossal nerve disease, Hypoglossal denervation, Yin-Yang sign, Yin-Yang tongue sign
Introduction
Yin-Yang is a typical ancient symbol in Chinese philosophy and religion that symbolizes two opposing forces that interact with each other but are harmonious. 1 The Yin-Yang sign was first used to depict the characteristic bidirectional colour blood flow of aneurysms on colour Doppler sonography. 2–4 Recently, the Yin-Yang sign was also used to describe the obvious contrast between the hyperdense contrast material–filled lumen and hypodense mural thrombus on contrast-enhanced CT scans. 1,5 The Yin-Yang sign of aneurysm, a useful diagnostic index, has been widely accepted by clinicians and radiologists for its vivid and impressive description of the characteristics of blood flow and thrombosis in true or false aneurysms. A similar black-and-white sign in patients with unilateral hypoglossal palsy on the cross-sectional images of denervated tongue was discovered in our research. To depict this change vividly, we described a Yin-Yang tongue sign based on the former image description. This performance is not a rare condition clinically and essentially represents tongue muscle atrophy caused by hypoglossal denervation. 6,7 During clinical image review, we found that many patients with Yin-Yang tongue signs also had HC lesions. Therefore, this retrospective study aimed to explore the causes of the Yin-Yang tongue sign and discuss its diagnostic value.
Methods and materials
This retrospective study was approved by the institutional review board, and written informed consent was waived for all patients. A total of 290 patients treated in our hospital from January 2014 to December 2020 were retrospectively reviewed. Clinical records, such as age, sex, physical examination, and imaging examination, were reviewed.
The inclusion criteria were as follows: (1) patients with unilateral HN deficits and physical examination to detect tongue midline displacement and tongue deviation when protruded; (2) CT or MR scan range covering the full length of HN and tongue muscle; and (3) complete medical histories and pathological results.
A total of 183 patients were excluded based on the following exclusion: (1) patients without CT or MR examination, or poor image quality; (2) patients with systemic diseases such as diabetes and autoimmune diseases; (3) patients with tongue deviation after operation or trauma; and (4) patients with bilateral tongue atrophy.
A total of 107 patients with clinically and pathologically confirmed HN palsy and tongue deviation were enroled in our study (47 females and 60 males, median age 54 years, age from 24 to 86 years). A total of 107 patients were further divided into two groups according to whether they had Yin-Yang tongue signs: the positive group (55 patients, 51.4%) and the negative group (52 patients, 48.6%) (Figure 1).
Figure 1.
Flowchart of patient enrolment. A total of 107 patients with tongue deviation in the HN pathway were enroled in the analysis. Fifty-five patients showed signs of Yin-Yang tongue, and fifty-two patients showed negative signs.
Scanning protocol
All brain and neck MR studies were performed on 3.0 T scanner (Discovery 750; GE Healthcare) using 8-channel head and neck coil or 32-channel head coil. MR routine sequences for the brain included: (1) axial T1WI and sagittal T1 FLAIR and (2) axial T2 FLAIR and T2W-PROPELLER. MR sequences for the neck included: (1) axial and sagittal fast spin-echo T1WI; (2) axial T2WI and T2-IDEAL images; and (3) coronal STIR. Axial serial sections that covered the entire anatomical length of the HN were obtained from a position across the skull base to the mandibular angle. Other parameters were as follows: slice thickness, 3.0–6.0 mm; slice spacing, 1.0–2.0 mm; a NEX of 1–2; FOV, 28 cm; and matrix, 320 × 192. Contrast-enhanced sagittal, coronal, and axial T1 fat-suppressed images were obtained after intravenous injection of Gd-DTPA (0.2 ml/kg). CT scan was performed using Canon Activion 16, and the scan range was from the head to the neck. The parameters were as follows: section thickness: 1.0–1.3 mm, tube current 220 mA, and tubular voltage 120 kV.
Image evaluation
Eighty patients underwent MR examination, and 27 patients had both CT and MR examinations. All the lesions detected by MRI or CT were blindly evaluated and assessed by two radiologists (with 10 years and 13 years of experience). The final assessments were judged by consensus.
The Yin-Yang tongue sign was described as unilateral tongue with significant atrophy or fat infiltration compared with the contralateral normal side-according to CT scans or MRI images. This sign (Figure 2) meets at least one of the following criteria: (1) CT: CT showed hypodensity of the involved hemitongue, the CT value was −45.0 ~ −1 HU, and the normal side showed soft tissue density; (2) MR: T1WI and T2WI showed hyperintensity on the involved side and iso- or hypointensity on the normal side. Postcontrast fat-saturated T1WI showed hypointensity of tongue muscle on the affected side and slightly enhanced tongue muscle signal on the normal side. Other signs of tongue denervation are not regarded as the criteria for judging the sign, such as the loss of volume of the hemitongue, the displacement of the midline of the tongue, and the protrusion of the base of the hemitongue into the oropharyngeal cavity.
Figure 2.
Typical feature of the Yin-Yang tongue sign. Imaging examination demonstrates tongue atrophy and fat infiltration of the left hemitongue of a 54-year-old female with schwannoma with a hyperintensity signal on T1WI (a), hypointensity signal on postcontrast fat-saturated T1WI (b), hyperintensity signal on T2WI (c), and hypodensity on CT scan (d).
Two experienced radiologists comprehensively assessed the location of HN lesions. HC involvement in the positive group was classified into two categories based on imaging findings: (1) HC dilation: Intermediate diameters (IDs) of the bilateral HCs were measured on axial images. The calculation formula was as follows: R = L/L0 (L = ID of the affected side, L0 = ID of the normal side). When R ≥ 1.5 and the bone cortex of HC was intact, HC dilation was considered (Figure 3 and Figure 4). (2) HC erosion: HC was occupied by an ill-defined mass and the bone cortex of HC was destroyed and replaced by tumour tissue on the CT image. Due to the destruction of the bone cortex of HCs, the R value was unavailable in this group (Figure 4).
Figure 3.
Measurement of ID of the bilateral HC. A. midpoint of internal diameter; B. midpoint of external diameter; H. midpoint of ID.
Figure 4.
Sample of HC dilation (a, arrow). Sample of HC erosion (b, arrow).
Statistical methods
All statistical analyses were performed by SPSS software (version 26.0). Continuous variables are expressed as mean or median, and categorical variables are expressed as percentages (%). Categorical variables were compared with the chi-squared test. The sensitivity, specificity, and accuracy of the Yin-Yang tongue sign for suggesting skull base lesions around HC in patients with tongue deviation were calculated. Interobserver agreement was analysed by κ test. Two-tailed p < 0.05 indicated that there was a significant difference.
Results
The final clinical diagnosis and characteristics of patients with tongue deviation are displayed in Table 1. HN involvement mainly occurred in the skull base (61.8%), skull base and carotid space (10.9%), and carotid space segment (12.7%). Neurogenic (50.9%), squamous cell carcinoma (14.5%), and metastases (12.7%) were the predominant aetiologies.
Table 1.
Clinical diagnosis and characteristics in patients with tongue deviation
| Patients with tongue deviation | Yin-Yang tongue sign | |
|---|---|---|
| Positive (n = 55) | Negative (n = 52) | |
| Sex (F/M) | 27/28 | 20/32 |
| Median age (interquartile range) | 54 (37 ~ 71) | 55 (40 ~ 70) |
| Involved segment (%) | ||
| Intracranial | 1 (1.8%) | 34 (65.4%) |
| cisternal | 3 (5.5%) | 2 (3.8%) |
| skull base | 34 (61.8%) | 6 (11.5%) |
| skull base and carotid space | 6 (10.9%) | 4 (7.7%) |
| carotid space | 7 (12.7%) | 2 (3.8%) |
| sublingual | 1 (1.8%) | 0 (0.0%) |
| unknown | 3 (5.5%) | 4 (7.7%) |
| Etiologies (%) | ||
| neurogenic tumours | 28 (50.9%) | 6 (11.5%) |
| cerebrovascular diseases | 1 (1.8%) | 25 (48.1%) |
| metastases | 7 (12.7%) | 4 (7.7%) |
| inflammatory lesions | 1 (1.8%) | 6 (11.5%) |
| squamous cell carcinoma | 8 (14.5%) | 1 (1.9%) |
| osteogenic tumours | 4 (7.3%) | 0 (0.0%) |
| amyotrophic lateral sclerosis | 1 (1.8%) | 1 (1.9%) |
| meningioma | 1 (1.8%) | 1 (1.9%) |
| adenoid cystic carcinoma | 1 (1.8%) | 0 (0.0%) |
| others | 3 (5.5%) | 8 (15.4%) |
The incidence of skull base lesions around HC was significantly higher in positive group than in the negative group (χ2: 30.730, p < 0.001). The sensitivity, specificity, and accuracy of the Yin-Yang tongue for suggesting skull base lesions around HC were 72.4%, 80.8%, and 76.6%, respectively (Table 2).
Table 2.
Yin-Yang tongue sign for suggesting skull base lesions around HC in patients with tongue deviation
| skull base segment (HC) involvement | Yin-Yang tongue sign | sensitivity | specificity | accuracy | |
|---|---|---|---|---|---|
| Positive (n = 55) | Negative (n = 52) | ||||
| Yes | 40 | 10 | 72.4% | 80.8% | 76.6% |
| No | 15 | 42 | |||
In our series, the interobserver agreement for the evaluation of HC dilation and HC erosion was excellent (κ coefficient: k = 0.842, p < 0.01 and k = 0.790, p < 0.01, respectively). There were two categories of HC involvement in the positive group: 21 cases of HC dilation (21/55, 38.2%), and 19 cases of HC erosion (19/55, 34.5%). HC dilation was all from benign tumours, including schwannomas (n = 18), paragangliomas (n = 2), neurofibroma (n = 1). And HC erosion was more prone to malignant lesions, including metastases (n = 7), squamous cell carcinoma (n = 4), and myxochondrosarcoma (n = 1). In addition, there were 7 cases of benign tumours with HC erosion, including chordomas (n = 3), paragangliomas (n = 2), schwannoma (n = 1), and phosphaturic mesenchymal tumour (n = 1). (Table 3).
Table 3.
The relationship between benign and malignant lesions and HC involvement
| HC involvement | R value | Nature of lesions | |
|---|---|---|---|
| Benign | Malignant | ||
| HC erosion | N/Aa | 21 | 0 |
| HC dilation | 2.84 (1.73 ~ 4.89) | 7 | 12 |
| Non-HC damage | 1.09 (0.91 ~ 1.30) | 10 | 5 |
N/A means data are unavailable.
Discussion
To our knowledge, the Yin-Yang tongue sign is a newly-proposed imaging semiology, that is used to describe asymmetric imaging of unilateral denervated tongues. With the midline of the tongue as a boundary, both sides of the tongue were innervated by unilateral HN. 8–10 CT or MR imaging of both sides of the tongue muscle was symmetrical. Hypoglossal denervation caused by unilateral HN injury can lead to hemitongue atrophy and fat infiltration, which presents evident contrast on CT or MR compared with the contralateral normal side. 6,8,11 This imaging appearance is similar to Yin-Yang symbols. Therefore, the Yin-Yang tongue sign can be used as a reliable, easily identifiable, and memorable imaging sign to describe this muscle denervation due to HN injury. We believe that this sign should be used as evidence pointing to lesions in the HN pathway.
HN involvement commonly occurs in the following segments: intracranial, cisternal, skull base, carotid space, and sublingual segment. 12 Fifty-one patients (92.7%) in the positive group had solid lesions in the pathway of the HN, which indicated that HN injury caused by the mass effect of solid lesions may be the most important cause of the Yin-Yang tongue sign. Our results showed that, relative to other segments of the HN, 40 cases (72.4%) have involved skull base segments in the positive group. The skull base is an intricate structure and is located at the edge of the routine imaging scan, which often leads to ignoring its abnormality by radiologists. 13,14 In a review of 9 cases of skull base lesions by Loevner, 13 5 of them manifested by HN palsy, and 2 cases exhibited tongue fat replacement, but all cases were initially evaluated as normal. Combarros et al 14 retrospectively reviewed 7 cases of hypoglossal denervation caused by skull base lesions and reported that all images were misinterpreted as normal or base-of-tongue tumours. Our investigation demonstrated that the Yin-Yang tongue sign has high sensitivity and specificity (72.4 and 80.8%, respectively) for localizing skull base lesions in patients with tongue deviation. When the Yin-Yang tongue sign is found, the possible aetiology should be systematically traced along the HN pathway, especially the skull base segment. In addition, it can help reduce misdiagnosis.
Multiple aetiologies in the HC region can interfere with the function of normal HN, including neurogenic tumours, malignancy infiltration, metastases, osteogenic tumours, and vascular compression. 12,15–18 In the positive group, the most common aetiology is neurogenic tumours (50.9%), including 21 cases of schwannomas, 6 cases of paragangliomas, and 1 case of neurofibroma. Both schwannoma and neurofibroma are benign neoplasms originating from the nerve sheath, while paragangliomas originate from the nerve crest of nonchromaffin cells. Paragangliomas are commonly seen in the lower part of the head and neck, such as carotid artery bifurcation, along the vagus nerve, at the jugular foramen, and in the middle ear, which can cause secondary involvement of HN. 16 Schwannomas account for 8% of intracranial tumours, and mainly involve the eighth cranial nerve. Although hypoglossal schwannomas are relatively uncommon, more than 2/3 of hypoglossal schwannomas are located at the skull base, passing through HC and dumbbell-shaped hypoglossal schwannomas are the most common type. 19–21
Direct invasion of squamous cell carcinoma (14.5%) is the second most common cause of the Yin-Yang tongue sign, especially nasopharyngeal carcinoma in the parapharyngeal space. In reports, approximately 13–25% of nasopharyngeal carcinoma patients have cranial nerve palsy at diagnosis. 22–24 Although nasopharyngeal carcinoma frequently involves the abducent nerve and trigeminal nerve, it can also grow posteriorly and inferiorly involving the perineural HC and cause HN injury by perineural infiltration. 24 In addition, skull base metastases (12.7%) in our research, including lung cancer (4 cases), hepatocellular carcinoma (2 cases), and gingival carcinoma (one case), can also cause HN injury and develop the Yin-Yang tongue sign. Primary bone tumours originating from the midline of the clivus, such as chordoma, can be accompanied by extensive osteolytic destruction and involve HC. 16
The HC involvement categories were evaluated in the positive group, in which HC dilation accounted for 38.2% of cases. Benign tumours originating from the nerve sheath showed eccentric growth centering on the nerve fibre and were more likely to push nerves aside causing relatively mild damage if there were no limitation of the bony structure. 20,21,25 Hypoglossal schwannomas in the skull base may expand HC by distensible growth (Figure 5). The hard bone tissue around the HC limits the long-term expansive growth of tumour, so compression from both neurogenic tumours and surrounding bone tissue is the most straightforward damage to the nerve fiber, which may be the primary reason for the Yin-Yang tongue sign. It has been reported that 50% of hypoglossal schwannomas extend through the HC and have a dumbbell-shaped appearance, which is a common type of tongue atrophy. 26 Weindling et al 27 reported that all 16 cases of hypoglossal schwannomas involved HC and HN. This is consistent with our findings. A total of 34.5% of cases showed HC erosion in the positive group. Malignant tumours such as nasopharyngeal carcinoma and metastases invade the skull base of the HC region, while the nerve sheath composed of multiple layers of collagen and basement membrane has resistance against invasion of skull base metastasis and the function of nerve fibres can remain intact. 28 This sign might be related to deep infiltration and recurrence of tumours. Therefore, we hypothesized that the morphological changes of HC may help to determine the benign or malignant mass.
Figure 5.
Schwannoma in a 28-year-old male with hearing loss, choking, and hoarseness for 4 months. Axial CT shows hypoattenuation of the left hemitongue and the CT value was −12 HU (a, asterisk). Axial CT (bone window) demonstrates left HC dilation with marginal osteosclerosis (b). Axial and sagittal postcontrast T1WI shows inhomogeneous enhancement of the dumbbell-shaped mass, which has an internal nonenhancing cystic focus (c and d, arrows).
Our study has a few limitations. First, the retrospective nature of the study limits the acquisition of radiological and medical history data. Second, we did not conduct further study on the effects of clinical courses on tongue denervation. Tongue atrophy and fat infiltration caused by denervation are asymptotic behaviours. Because the clinical symptoms have some degrees of subjectivity, it is difficult to judge the initial time of nerve damage. Third, because of the limited sample size, we were unable to perform a comprehensive statistical analysis of the correlation between morphological changes in HC and the benignity of the mass. In subsequent studies, we will expand the sample size.
In conclusion, the Yin-Yang tongue sign is formed by unilateral tongue atrophy and fat infiltration caused by lesions in the HN pathway, especially those invasive or compressive lesions involving the skull base segment. Therefore, proper awareness of the Yin-Yang tongue sign can help to reduce misdiagnosis of neurogenic tumours and malignancy infiltration involving perineural HC.
Footnotes
Acknowledgements: The authors thank Prof. Zhiyun Yang, Department of Radiology, First Affiliated Hospital of Sun Yat-Sen University, Guangzhou, P.R.China, for her suggestion and support. This study has received funding by the Society of China University Journals (CUJS-YX-2021-3-3).
The authors Jian Guan and Chu Pan contributed equally to the work.
Contributors: Xuexia Chen: Data curation, Investigation, Methodology, Software, Visualization, Roles/Writing - original draft. Jingru Yi: Data curation, Software, Investigation. Simin Liu: Supervision, Visualization. Weiwei Chen: Supervision, Visualization. Jian Guan: Conceptualization, Formal analysis, Resources, Validation, Visualization, Writing - review & editing. Chu Pan: Conceptualization, Formal analysis, Methodology, Resources, Validation, Visualization, Writing - review & editing.
Contributor Information
Xuexia Chen, Email: 1043462138@qq.com.
Jingru Yi, Email: 2305377713@qq.com.
Simin Liu, Email: liusm117@163.com.
Weiwei Chen, Email: Chenweiwei_tjh@163.com.
Jian Guan, Email: guanj6@mail.sysu.edu.cn.
Chu Pan, Email: panchu@21cn.com.
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