Abstract
Total laryngectomy is the primary treatment for locally advanced laryngeal carcinomas. However, routine thyroid removal (total or hemithyroidectomy) during this procedure is controversial, as the incidence of thyroid gland involvement varies and may lead to lifelong thyroid supplementation, increasing postoperative morbidity. The lack of a consensus on managing the thyroid gland in laryngeal carcinoma cases necessitates improved evaluation techniques, with radiology playing a crucial role in this aspect. Understanding the correlation between radiological factors and histopathological involvement of the thyroid gland can aid in formulating appropriate management strategies during total laryngectomy. To study the correlation of preoperative radiological factors with histopathological involvement of thyroid gland in laryngeal carcinomas. This was a retrospective study which included 57 patients who underwent total laryngectomy for squamous cell carcinoma of larynx. The pre-operative CT findings such as involvement of thyroid cartilage, cricoid cartilage, paraglottic space, anterior commissure, subglottis and thyroid gland along with transglottic extension of tumor were correlated with post-operative histopathological thyroid gland involvement. Cricoid cartilage erosion and thyroid gland involvement in CT scans individually exhibited positive likelihood ratios of 2.58 and 3.23, respectively, demonstrating a reasonable agreement with histopathological findings. The specificity of cricoid cartilage and thyroid gland involvement was also higher with values of 76.4% and 81%, respectively. Moreover, combining thyroid and cricoid cartilage erosion in CT scans as a predictive parameter for thyroid gland involvement resulted in a better likelihood ratio of 8.23 and a fair agreement with histopathological findings. We conclude that cricoid cartilage erosion and thyroid gland involvement in pre-operative CECT can be taken as a preoperative indicator for intraoperative decision on thyroidectomy.
Keywords: Carcinoma larynx, Total laryngectomy, Thyroidectomy, Contrast enhanced computed tomography of neck
Introduction
Total laryngectomy is considered as the best treatment modality for locally advanced laryngeal carcinomas. This procedure involves complete removal of the larynx with hemi or total thyroidectomy. There is no universally accepted consensus in dealing with the thyroid gland in case of carcinoma of the larynx. Hence, it is important to look into the factors that can predict thyroid gland involvement in glottic cancers.
The incidence of thyroid gland involvement in laryngeal cancer ranges from 0 to 23%, the value of which is derived based on the histopathological study of post-operative total laryngectomy specimens [1]. Total thyroidectomy necessitates lifelong thyroid supplementation, adding on to the post operative morbidity due to laryngectomy [2]. Preservation of one of the lobes of the thyroid gland can lead to a lower incidence of post operative hypothyroidism. Unnecessary removal of the thyroid gland is being done in over 90% of patients undergoing total laryngectomy [3].
The management of the ipsilateral thyroid lobe during total laryngectomy for laryngeal squamous cell carcinoma lacks consensus. Radiology plays a significant role in evaluating laryngeal carcinoma cases, with various radiological factors aiding in treatment plan decisions regarding the thyroid gland and identifying pathological thyroid gland involvement. Thus, determining its correlation with preoperative radiological factors shall help us frame strategies that help in deciding on the management of thyroid gland in dealing with operable laryngeal malignancies.
The objective of our study was to study the correlation of preoperative radiological factors with histological involvement of thyroid gland in laryngeal carcinomas.
Materials and Methods
This is a retrospective study that reviewed the histopathological correlation of thyroid gland involvement in laryngeal carcinomas with a few other radiological parameters in preoperative Contrast Enhanced Computed Tomography(CECT) study. All provisions of the Declaration of Helsinki were followed. All the patients who were treated with total laryngectomy for squamous cell carcinoma between 2013 and 2019 in our institute were included in our study. We found 57 patients who underwent total laryngectomy fulfilled the inclusion and exclusion criteria with clinical case records fully complete for data retrieval.
The parameters studied included age, gender, preoperative radiotherapy status, preoperative CECT (taken within 1 month prior to surgery) findings, TNM classification, post-operative histopathology .
In our institute, the nature of thyroidectomy and its extent was determined by the clinical and radiological extension of the disease to the thyroid gland. In addition, anterior commissure involvement and subglottic extension (> 10 mm) were also taken as criterion to consider total thyroidectomy. Hemithyroidectomy was done in our centre for resecting out the occult metastases that may be present in the ipsilateral thyroid lobe in patients with suspicious radiological features such as close proximity to tumor. TNM staging used in our study was based on the 7th edition of American Joint Committee on Cancer staging manual. Post operative biopsy report of all the 57 patients were reviewed and thyroid gland involvement was noted. The pre-operative CT findings were assessed for involvement of thyroid cartilage, cricoid cartilage, paraglottic space, anterior commissure, subglottis and thyroid gland along with transglottic extension (Table 1). The preoperative CT findings were correlated with post-operative histopathological reports.
Table 1.
Radiological parameters assessed in the study
| PARAMETER | STANDARDISATION FOR RADIOLOGY |
|---|---|
| Subglottic extension | > 10 mm [1] |
| Anterior commissure(depth) |
GRACI signs were recognized by the following: 1. At the horizontal plane on a coronal image, presence of anterior vocal commissure thickening greater than 1.0 mm detected in at least two contiguous tomographic slices 2. At the vertical plane on sagittal reconstruction, presence of AVC tumor volume growing superiorly to the preepiglottic space, or anteriorly to the thyroid cartilage, or inferiorly to the cricoid cartilage [4]. |
| Transglottic tumor | Transglottic tumor is a term used to describe tumors encroaching on both glottis and supraglottis with or without subglottic components and when the site of origin is unclear (these usually develop from glottic tumors) [5]. |
| Paraglottic space | Fat tissue planes not preserved between the glottis and thyroarytenoid muscle |
| Thyroid gland involvement | Heterogenous enhancing lesion with thyroid gland enlargement |
| Thyroid cartilage erosion | Sclerosis, erosion |
| Cricoid cartilage | Sclerosis, erosion |
Results
A total of 57 cases who underwent total laryngectomy for squamous cell carcinoma of larynx during our study period were included in the study. The total number of males were 54 and females were 3 (Table 2). The mean age of the patients in our study population was 63 years and majority of them were males (94.7%).
Table 2.
The nature of thyroidectomy performed in the study subjects
| Nature of thyroidectomy | Frequency |
|---|---|
| Total thyroidectomy | 34 |
| Hemithyroidectomy | 14 |
Of the 57 cases, Total thyroidectomy was done in 34 patients and hemithyroidectomy was done in 14 patients and thyroid was preserved in 9 cases. (Table 2)
On preoperative evaluation, 9 patients had evidence of radiological thyroid involvement by the tumour among which only 3 patients had histological involvement of thyroid gland. CECT of the patients who had histological involvement of thyroid gland as well as those who did not have histological involvement were reviewed in detail retrospectively and the pattern of thyroid gland involvement and presence of other radiological parameters were looked into (Table 1). Among the patients who underwent thyroidectomy (hemi/ total), 39 patients had no evidence of radiological thyroid gland involvement, two patients were found to have histopathological involvement of thyroid gland (Table 3).
Table 3.
Correlation of pre operative radiology and post operative histology of thyroid gland among patients who underwent thyroidectomy (n = 48)
| Radiologically positive | Radiologically negative | |
|---|---|---|
| Biopsy positive | 3 | 2 |
| Biopsy negative | 6 | 37 |
The radiological features that were looked into in our study were thyroid gland involvement, thyroid and cricoid cartilage erosion, paraglottic space involvement, subglottic extension, anterior commissure involvement and transglottic tumours. Percentage of these radiological features in the study population in whom thyroid gland was addressed and radiological thyroid gland invasion in association with each of them were estimated (Table 4).
Table 4.
Percentage of occurrence of radiological parameters in the study population, with the percentage of radiological involvement of thyroid gland
| Sl no. | Radiological parameter studied | Occurrence in the study population (%) | Radiological thyroid gland involvement (%) |
|---|---|---|---|
| 1 | Thyroid cartilage erosion | 66.66 | 15.63 |
| 2 | Paraglottic space involvement | 70.83 | 14.71 |
| 3 | Anterior Commissure involvement | 54.17 | 11.54 |
| 4 | Subglottic extension | 56.25 | 11.11 |
| 5 | Transglottic tumour | 39.58 | 10.52 |
| 6 | Cricoid cartilage erosion | 27.08 | 23 |
This was followed by calculation of sensitivity and specificity of these radiological factors in histological thyroid gland involvement along with positive and negative likelihood ratio (LR) and agreement of these factors with thyroid gland invasion histologically (Table 5). Agreement between radiological parameters and histopathological thyroid gland involvement were estimated using the Kappa statistics (Kappa value: 0.00 to 0.20 -slight agreement, 0.21–0.4-fair agreement, 0.4–0.6 = moderate agreement, 0.6–08 = substantial agreement, 0.8–1.0 = almost perfect) [6].
Table 5.
Predictive sensitivity and specificity of thyroid gland involvement in relation to radiological parameters, with the positive and negative likelihood ratios and kappa agreement
| Radiological parameter involved | Sensitivity | Specificity | Positive LR * | Negative LR* | Kappa Agreement |
|---|---|---|---|---|---|
| Thyroid Cartilage | 100 | 37.5 | 1.59 | 0 | Slight (0.11) |
| Paraglottic Space | 100 | 32.56 | 1.48 | 0 | Slight (0.091) |
| AVC | 60 | 46.51 | 1.12 | 0.86 | Slight (0.023) |
| Subglottic Extension | 60 | 44.5 | 1.07 | 0.91 | Slight (0.014) |
| Transglottic Tumours | 40 | 60.47 | 1.01 | 0.99 | Slight (0.002) |
| Cricoid Cartilage | 60 | 76.74 | 2.58 | 0.52 | Fair (0.215) |
| Thyroid Gland | 60 | 81.40 | 3.23 | 0.49 | Fair (0.271) |
| Anterior Commissure and Subglottis | 60 | 58.14 | 1.43 | 0.69 | Slight (0.075) |
| Anterior Commissure, Subglottis and Thyroid gland | 40 | 90.7 | 4.3 | 0.66 | Fair (0.238) |
| Thyroid cartilage and Cricoid cartilage erosion | 60 | 93 | 8.6 | 0.43 | Moderate(0.49) |
*LR = Likelihood ratio
(Note:Sensitivity and specificity have been calculated with 95% confidence interval. Sensitivity and specificity don’t hold valid for a few individual parameters like thyroid cartilage erosion and paraglottic space involvement. Negative LR for both these is 0 which is not statistically acceptable)
Among 48 patients who underwent thyroidectomy (total and hemi included), 32 of them showed radiological thyroid cartilage involvement. All 5 patients who had histopathological involvement of thyroid gland had radiological thyroid cartilage involvement. This amounts to 100% sensitivity and a specificity of 37.5%. This value of 100% is not acceptable as this might be a coincidental. Among our study population, 66.66% showed radiological thyroid cartilage erosion, out of which 15.63% of patients had histopathologically positive thyroid gland.
A total of 34 (70.83%) patients had paraglottic space involvement in our study population. All 5 patients who had histopathological gland involvement had paraglottic space involvement on CT amounting to a predictive sensitivity of 100% and specificity of 32.5%.
Out of 26 patients having anterior commissure involvement (54.17%), 3 patients (11.53%) had histopathological thyroid gland involvement, the senstivity and specificity being 60% and 46.5% respectively.
Among 27 patients (56.25%) with subglottic extension, 3 patients (11.11%) had histopathological thyroid gland involvement with sensitivity and specificity being 60% and 44.5% respectively. Amidst 19 patients (39.58%)with trangslottic extension, 2 patients (10.52) had thyroid gland involvement, with sensitivity being 40% and specificity being 60.4%. In 13 patients(27.08%) with cricoid cartilage involvement radiologically, 3 patients(23%) had histopathological involvement of thyroid gland, with a sensitvity and specificity of 60% and 76.4% respectively. In 9 patients(18.75%) with radiological involvement of thyroid gland, 3 patients(10.42%) with histopathological thyroid gland involvement had radiological evidence of metastases to thyroid gland bringing sensitivity to 60% and specificity to 81%.
Among the radiological parameters studied, radiological thyroid cartilage erosion, paraglottic space involvement, anterior vocal commissure involvement, subglottic extension and transglottic tumours had a low positive likelihood ratio less than 2 and all these factors showed only slight agreement with histopathological thyroid gland involvement. Cricoid cartilage erosion and thyroid gland involvement in CECT as individual parameters showed better positive likelihood ratios of 2.58 and 3.23 respectively which was in fair agreement with biopsy positive thyroid gland.
Considering combined thyroid and cricoid cartilage erosion in CECT as a predictive parameter for thyroid gland involvement, it showed a better likelihood ratio of 8.23 and fair agreement with histopathological thyroid gland involvement. Combined radiological anterior commissure involvement and subglottic extension showed a positive likelihood ratio of 4.3 and moderate agreement with thyroid gland positivity on histopathological examination.
Among the various radiological parameters listed, thyroid cartilage and paraglottic space involvement had sensitivity of 100% but specificity is low; so they cannot be taken as an individual parameter of assessment. But, the individual specificity of cricoid cartilage and thyroid gland involvement is higher when compared to other parameters which accounted to 76.4% and 81% respectively.
Discussion
Our study was a retrospective account of 57 total laryngectomies and the conclusions drawn from our study has a great significance as these can be extrapolated into future surgical practice. As the query on hemi or total thyroidectomy in total laryngectomy for carcinoma larynx remains unanswered, the findings of our study can be considered while planning thyroid gland treatment in the manangement of laryngeal carcinomas.
Total laryngectomy is the gold standard in the management of locally advanced laryngeal carcinomas [7]. This procedure significantly affects the quality of life of patients considering the possible morbidities like alaryngeal speech, olfactory impairment, permanent end tracheostomy and hypothyroidism. Thyroidectomy as a part of laryngectomy inevitably leads to post operative hypothyroidism which is further accentuated by post-operative irradiation [8]. The incidence of hypothyroidism following total laryngectomy is 32–89% which is detrimental for patients with less access for thyroid hormone replacement and regular follow-up [9]. The incidence of hypothyroidism in our study was 48% which falls within this range. Hypothyroidism leads to cardiac morbidity, post-operative depression, constipation, skin dryness, delayed wound healing, pharyngeal fistula, massive head and neck oedema and also has an adverse effect on voice rehabilitation for the patient [10, 11]. Preserving the thyroid lobe can also improve parathyroid preservation and enhance the neopharyngeal closure [12].The benefit of preserving the thyroid gland lies primarily in the immediate postoperative period were the above mentioned complications can be mitigated and can have a positive impact on the final outcome of the patient. This points to the significance of detailed preoperative planning on thyroid gland management in patients who undergo total laryngectomy for carcinomas of the larynx.
Our study looked into the detailed evaluation of radiological features in CECT images of the larynx and their association with histopathological involvement of thyroid gland so as to clear the surgeon’s perspective on treating the thyroid gland during total laryngectomy.
Thyroid gland involvement in laryngeal cancer is due to the proximity of the thyroid gland to the larynx [10].Spread of cancer to the thyroid gland can occur by three routes- Direct, Hematogenous and lymphatic spread. Tucker had explained that the laryngeal compartments determines how the cancer spreads and that they spread through the zones of least resistance [13]. Laryngeal regions most susceptible to spread are cricothyroid membrane and angle of the thyroid cartilage [14]. The most frequent method of spread to the thyroid gland is by direct extension [15].
The thyroid gland being vascular can facilitate metastases if involved. Previous studies have found early recurrences in cases where thyroid gland was involved [7]. Invasion of thyroid gland by laryngeal squamous cell cancer is a poor prognostic sign in laryngeal squamous cell carcinoma [15]. The thyroid gland is removed routinely during laryngectomy to achieve adequate tumor-free margins, to remove occult metastases to the thyroid gland from larynx and to gain access to the lymph nodes in the tracheoesophageal groove. High peristomal recurrences have been reported with subglottic cancers where thyroid glands were preserved. Inspite of all the above indications, very often studies have indicated that the removal of the thyroid gland is more than the actual oncological requirement. Thus, a strategic method needs to be devised for preserving the thyroid gland during total laryngectomy.
Our study has an incidence of thyroid gland involvement of 10.41% which is in concordance with other studies, such as Kumar et al. showing 10.7% and Brennan showing 8% involvement, gillardin et al. showing 13% [3, 8, 15].
In our study, we found that in all cases where histological thyroid gland invasion was present, there was paraglottic space involvement in preoperative CT. Our findings were supported by Brennan et al. who states paraglottic space involvement as the most important criteria for thyroid gland involvement. The main content of the paraglottic space is fat which provides an important route for the spread of cancer. Thus, paraglottic space is considered to be a detrimental factor for the spread of tumour in the anteroinferior direction but on the downside, paraglottic space involvement in our study was present in 29 out of 48 patients who underwent total laryngectomy with hemithyroidectomy or total thyroidectomy, where the thyroid gland turned out to be normal thus reducing its specificity to 32.5%. Hence, in our study, paraglottic space could not be used as a reliable factor to predict thyroid gland involvement .
Though thyroid cartilage involvement in preoperative CT was present in all cases were thyroid gland involvement was found (sensitivity 100%), it is rare to find an isolated thyroid cartilage involvement without subglottic or transglottic involvement thus making validation difficult for thyroid cartilage to be an independent criteria for thyroidectomy. This finding is supported by Mendelson et al. [1].
Agazadeh et al. have given a statistically significant relationship between anterior commissure involvement and thyroid gland invasion where 11 out of 12 thyroid gland involved specimens had anterior commissure involvement but our study does not give a significant relationship between them (sensitivity 60% and specificity 43.5%) [16]. Our findings were in concordance with sandeep nayak et al. who states that anterior commissure involvement cannot be taken as a criteria for thyroidectomy as the distance between anterior commissure and isthmus is about 2–3 cm.
Sandeep nayak et al. focuses on the the relation of transglottic tumours to thyroid gland as transglottic tumours being large volume tumours have propensity for lateral spread but our study does not find a significant relation between them with a sensitivity of 40% and specificity of 60.4% [7].
Sparano et al. have stressed the relationship between subglottic space and thyroid gland involvement were all cases of squamous cell carcinoma of glottis with direct extension to thyroid gland had subglottic extension [2]. The importance of subglotttic space can be inferred from the fact that the lymphatic drainage of the subglottic region passes through the thyroid gland thus serving as a route for spread but our study does not find a significant relationship between them (sensitivity 60% and specificity 44.5%).
We also observed that though cricoid cartilage was involved in 60% of cases were thyroid gland was affected, the proportion of cricoid cartilage involvement in histologically normal thyroid gland was low. This gives higher specificity rate of 76.74% for cricoid cartilage involvement. This finding is supported by Gaillardin et al. who demonstrated a statistically significant correlation between cricoid cartilage destruction on CT and histological thyroid gland invasion. In their study, slightly more than 40% of patients with CT signs of cricoid cartilage destruction had histological thyroid gland invasion.
When preoperative CT for thyroid gland was normal, histological thyroid gland invasion was present only in 4%. Thus, the need for thyroidectomy in a radiologically normal thyroid gland must be reassessed. On the bases of our study results, we infer that thyroidectomy can be done when there is thyroid gland invasion and cricoid cartilage destruction in preoperative CT. These results are supported by the study done by gillardin et al. [8]. Thus, 90% of the thyroid gland removed were histologically normal, similar findings were in other studies like Sparano et al., Biel et al., Ceyan et al. [2, 17, 18].
No significant association could be found between individual parameters of thyroid cartilage erosion, subglottic extension, transglottic tumour and anterior commissure involvement in CECT and histological thyroid gland involvement. Radiological cricoid cartilage erosion and thyroid gland invasion had better agreement and positive likelihood ratio for a histologically positive thyroid gland in laryngeal carcinomas. A combination of thyroid and cricoid cartilage erosion and anterior commissure,subglottic and thyroid gland involvement in CECT were better predictors of thyroid glandular invasion by the tumour.
Radiological involvement of thyroid gland but a histopathologically normal thyroid gland were noted in 6 cases. On retrospective inspection of these cases, following observations were made. In one patient, there was heterogeneously enhancing soft tissue density that displaces the upper pole of the left lobe of thyroid gland with loss of plane but direct involvement of the gland was not present (Fig. 1A). Another patient who was reported as radiologically positive had heterogeneously enhancing lesion with erosion of thyroid lamina and extra laryngeal tumor spread and loss of fat planes with upper part of left lobe of thyroid gland; direct involvement of gland not seen (Fig. 1B).
Fig. 1.
CECT neck axial cuts showing A Heterogenously enhancing soft tissue density displacing the upper pole of left lobe with significant loss of fat planes with rest of the gland (marked as asterix) B Heterogeneously enhancing lesion with erosion of thyroid lamina and extra laryngeal tumor spread (marked as yellow arrow) and loss of fat planes with upper part of left lobe of thyroid gland, direct involvement of gland not seen (marked as asterix)
In another patient, CT images clearly revealed extensive extralaryngeal extension and subglottic spread but maintained fat planes with upper part of left lobe of thyroid (Fig. 2A).
Fig. 2.
CECT neck axial cuts showing A Laryngeal tumour with subglottic extension (marked in yellow arrow) and extralaryngeal spread (marked in red arrow) with cricoid cartilage erosion
B heterogenously enhancing lesion (marked in asterix) in close proximity to the upper pole of right lobe of thyroid with an intervening fat plane of thickness < 1 mm on the right side with prominent vessel on the right side (marked as arrow)
Another interesting finding in one of the CTs was that tumour was in close proximity to the upper pole of thyroid gland with an intervening fat plane of thickness < 1 mm and vessel in between the laryngeal tumour and thyroid gland (Fig. 2B).
A retrospective inspection of the thyroid gland in yet another preoperative CT images revealed an isolated involvement of the isthmus region of the gland which could be an artefact due to previous tracheostomy. In those images, this artefact could have occurred due to the manipulation of thyroid isthmus which can be in the form of superior retraction of the isthmus. (Fig. 3)
Fig. 3.
CECT neck axial cuts showing involvement of isthmus of the thyroid gland (marked as arrow), but not in continuation with the laryngeal tumour, probably artefact secondary to previous tracheostomy
Thus, radiological involvement of thyroid gland requires guarded reporting. It is not only essential to analyse the contiguity of the thyroid lesion with the laryngeal lesion but also imperative to look for radiological involvement of the gland as denoted by irregular interface, distorted fat planes and direct tumor invasion.
Though previous studies have drawn up similar conclusions, the uniqueness of our study is in the fact that retrospective inspection of false positive cases ( radiologically positive and histologically negative) were done and established factors that are to be seen carefully while reporting glandular involvement. However, our study was limited by individual variations in radiological reporting. Even artefacts due to prior tracheostomy were considered as radiologically positive thyroid gland.
Conclusion
Our study pointed to the fact that patients with radiological involvement of cricoid cartilage and thyroid gland had greater incidence of pathological thyroid gland involvement. Hence, we conclude that cricoid cartilage erosion and thyroid gland involvement in pre-operative CECT can be taken as a preoperative indicator for intraoperative decision on thyroidectomy. Radiological involvement of gland is denoted by irregular interface, distorted fat planes and direct tumor invasion. Hemithyroidectomy can be preferred over total thyroidectomy in lateralised lesions of the glottis, where there is radiological sparing of cricoid cartilage and thyroid gland per se. Meticulous reporting is required in tracheostomized patients due to architectural distortion of isthmus of thyroid. Proper planning is facilitated by thorough evaluation of preoperative CECT parameters. Thus, a coordinated effort by the otolaryngologist and radiologist would lead to less morbid post-operative period in laryngectomies due to better treatment of the thyroid gland.
Acknowledgements
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