Selecting the Right Plane of Dissection in Thyroidectomy: Along the Recurrent Laryngeal Nerve or the Thyroid Capsule? A Retrospective Analysis.

Introduction  Total thyroidectomy remains highly technical, with a significant risk of recurrent laryngeal nerve (RLN) compromise and hypoparathyroidism. After identifying RLN, at the level of the ligament of Berry, local factors may compel the surgeon to either dissect along the nerve or the thyroid capsule. Objective  The objective of the present study is to compare these two approaches in terms of outcomes and complication rates. Methods  This is a retrospective analysis from September, 2013 to April 2019 of 511 consecutive patients undergoing thyroidectomy. General demographics and disease parameters were recorded. At the discretion of the surgeon and according to the demands of the local operative factors, the patients either had dissection along the RLN or along the thyroid capsule. Perioperative and postoperative parameters such as blood loss, duration of surgery, hospital stay, pain scores, analgesia requirements and complications were recorded. The groups were compared with the Pearson chi-squared test or with the Fisher exact test. A p-value < 0.05 was considered statistically significant. Results  The incidence of transient hypocalcaemia and transient RLN compromise were higher when dissection was performed along the nerve as opposed to the plane along the thyroid capsule. Other parameters including operative time, hospital stay, pain scores, analgesia requirement, wound infection, seroma, hemorrhage, and recurrence did not differ between the groups. Subgroup analysis of the patients who presented with complications showed that local factors, malignancy, and extent of surgery correlated positively with complications when dissected along the RLN. Conclusion  Dissection along the capsule of the thyroid during thyroidectomy is a safer plane in terms of low rate of transient RLN injury and hypoparathyroidism as opposed to dissection along the nerve. Fundação Otorrinolaringologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commecial purposes, or adapted, remixed, transformed or built upon. ( https://creativecommons.org/licenses/by-nc-nd/4.0/ ).

Introduction

Thyroid surgery remains a highly demanding and technical operation, despite the availability of modern technology. 1 2 3 Postoperative hypoparathyroidism and recurrent laryngeal nerve (RLN) paralysis are still heavily feared complications, and reasons for these are multifactorial. 4 5 6 There is a documented incidence of between 0.3 and 1.5% for permanent RLN paralysis, and of up to 10% for transient RLN compromise. 7 8 Surgeon experience, quality of training, and dissection skills remain important determinants of the operative outcomes. 9 Additionally, anatomical variations, functional status of the thyroid, and malignant pathology also have a certain role to play in the outcomes of this surgery. 10 11 12 13

There are numerous techniques currently being practiced to dissect in this area and to avoid injury to the RLNs and to the parathyroid glands. 11 14 The most common approaches are the lateral, inferior, superior, and superomedial approaches. 15 16 All these techniques have their own advantages and limitations; however, there is consensus among the endocrine surgeons that dissection of the nerve around the area along the ligament of Berry can be the trickiest part of the operation. 15

During the inferior and lateral approach, identification of the RLN remains a crucial step. 16 At this juncture, the dissection can move either along the nerve or the capsule, but at this point, many local factors, anatomical variations, fibrosis, adhesions, and malignant invasions can all play a significant role in the choice of the plane. 17 18 Remaining medially along the capsule has advantage of avoiding devascularization of the parathyroids and possibly of the nerve; however, with a higher incidence of leaving a small portion of residual thyroid tissue along the ligament of Berry. This might be acceptable for a benign pathology, but may not be for a malignant pathology in which complete resection of the thyroid tissue is the priority. On the other hand, dissection along the nerve provides dissection under vision, but makes the RLN vulnerable to traction, cautery, and devascularization injuries. 7 8 This also increases the chances of devascularization of the parathyroid glands, which, in many instances, lie very close to the capsule of the gland. Figure 1 depicts these plane choices in detail. Anatomical variations, toxicity, fibrosis or adhesions related to inflammation of a malignant pathology further add to the complexity of dissection in this area. In the present study, we evaluate the pros and cons of these two planes of dissection in clinical setting in terms of rate of complications.

Fig. 1

The picture explains the two planes at the level of ligament of Berry, that is, a plane along the recurrent laryngeal nerve (RLN) shown by the yellow line and a tissue dissection plane which is along the thyroid capsule and medial to recurrent laryngeal nerve (shown by the green line). Figure 1a clearly shows that adopting a tissue dissection plane along the capsule can help in saving inferior parathyroid (IP) and superior parathyroid (SP) without devascularizing them. It also avoids traction, diathermy and manipulation injuries to the RLN. Following this technique may leave some residual thyroid tissue (RT) in few cases, as shown in Figure 1d . Dissection along the nerve has the advantage of better exposure, which may be required in many cases to avoid injury to RLN, for example, in Figure 1c , where there are two branches of RLN.

Patients and Methods

Following ethical approval from the local institutional board, records of the patients undergoing thyroidectomy at a tertiary care center were reviewed. A total of 511 patients who were operated on over the course of 6 years from September, 2013 to April 2019. were included in the present study. General demographics of the patients and disease parameters were recorded. The RLN was routinely identified in all patients, and they were divided into two groups based on the dissection technique of RLN close to the ligament of Berry; in Group 1, dissection was performed along the nerve, and in Group 2, dissection was performed along the thyroid capsule. Groups 1 and 2 included 255 and 256, patients respectively. Both surgical techniques were used concurrently, and local factors guided the surgeons to opt for either technique. The present study includes the work of only two surgeons, hence minimizing variation in operational technique and performance. Neuromonitoring was not employed.

Serum calcium and parathormone (PTH) samples were drawn 48 hours after surgery. Transient postoperative hypocalcaemia was defined as single setting corrected calcium level < 8.5mg/dl (normal: 8.5-10.5mg/dl). On the 1 st postoperative day, flexible fiberoptic laryngoscopy was performed to assess vocal cord function, if clinically indicated. Hypocalcemia and RLN compromise were considered permanent if they persisted for > 12 months. Perioperative and postoperative surgical care parameters such as blood loss, duration of surgery, drain output, hospital stay, pain scores, analgesia requirements, and complications were reviewed and tabulated. The data were analyzed through IBM SPSS Statistics for Windows, version 21.0 (IBM Corp., Armonk, TX, USA). Means, standard deviations (SDs), and frequencies were measured as appropriate. Means were compared through the Mann-Whittney U t-test or through the Kruskal-Wallis test as statistically appropriate. The categorical data of the groups were compared with the Pearson chi-squared test 2 or with the Fisher exact test as statistically appropriate. A p-value < 0.05 was considered statistically significant.

Results

The general characteristics of the patients enrolled in the present retrospective study are summarized in Table 1 . They have been divided into two groups, and their characteristics are quite homogenous.

Table 1

General Characteristics of the Patients participating in the study

Measurement Parameter		Group 1(Dissection along the nerve)(n =  255 )	Group 2(Dissection along the thyroid capsule)(n =  256 )
Age (years old)		49.07 ± 11.73	47.96 ± 11.13
Gender
	Female	207 (81.2%)	209 (81.6%)
	Male	48 (18.8%)	47 (18.4%)
Clinical Diagnosis
	Follicular CA	12 (4.7%)	20 (7.6%)
	MNG (including Toxic)	13 (5.1%)	8 (3.06%)
	MNG involving Single Lobe	14 (5.4%)	16 (6.1%)
	Papillary CA	119 (46.6%)	108 (41.3%)
	Suspicious Solitary Nodule	78 (30.5%)	83 (31.8%)
	Primary Thyrotoxicosis	9 (3%)	12 (4.5%)
	Toxic Adenoma	10 (3.9%)	14 (5.3%)
Histological Diagnosis
	Benign Follicular Lesion	83 (32%)	87 (33%)
	Benign Hyperplastic Glands	32(12%)	34 (13%)
	Follicular Carcinoma	16 (6%)	24 (9%)
	Papillary Carcinoma	124 (48%)	115 (44%)
	Hashimoto's Thyroiditis	0	1 (0.3%)
Clinical Status
	Euthyroid	206 (80.7%)	201 (78.5%)
	Hypothyroid	3 (1%)	2 (0.7%)
	Hyperthyroid	46 (18.03%)	52 (20.3%)
ASA Status
	ASA-I	225 (88.2%)	229 (87.7%)
	ASA-II	15 (5.8%)	11 (4.2%)
	ASA-III	12 (4.7%)	9 (3.4%)
	ASA-IV	3 (1.1%)	7 (2.6%)
Gland Size WHO Classification (1974)
	WHO Class I	8 (3.1%)	13 (4.9%)
	WHO Class II	7 (8.75%)	1 (0.3%)
	WHO Class III	205 (80.4%)	202 (77.3%)
	WHO Class IV	35 (13.7%)	7 (2.6%)
Type of surgery
	Lobectomy and Isthmectomy	92(36.0%)	99(37.93%)
	Total Thyroidectomy	136(53.3%)	127 (48.6%)
	Completion Thyroidectomy	8 (3.1%)	13 (4.9%)
	Total thyroidectomy + Neck Dissection	19 (7.4%)	17 (6.5%)

Abbreviations: WHO, World Health Organization; CA, cancer; MNG, multinodular goiter; ASA, American Society of Anesthesiology.

Surgical care parameters and complications are documented in Table 2 . The incidence of transient hypocalcemia ( p  = 0.006) and of transient RLN compromise ( p  = 0.0001) were higher when the dissection was performed along the nerve when compared with dissection performed on the plane along the thyroid capsule. A total of 58 patients developed transient hypocalcemia, 45 from Group 1 versus 13 from Group 2. The rate of transient hypocalcemia was 17.6% in Group 1 versus 5.1% in Group 2 ( p

Table 2

Study endpoints summarized in both groups with and without drain

Measurement parameter	Group 1(Dissection along the nerve)(n =  255 )	Group 2(Dissection along the thyroid capsule)(n =  256 )	p-value
Mean length of surgery (minutes)	119.09 ± 38.26	117.15 ± 41.01	0.451
Perioperative mean blood loss	44.72 ± 26.03	37.52 ± 22.50	0.061
Postoperative Drain Output	53.22 ± 42.98	53.94 ± 33.75	0.146
Mean length of postoperative stay (hours)	34.91 ± 12.83	34.69 ± 12.75	0.219
Mean pain score (maximum = 10)	3.1 ± 1.1	2.3 ± 0.4	0.052
Median postoperative analgesic requirements according to the WHO pain ladder	Level II	Level II	0.321
Complications
Wound infection	8 (3.1%)	5 (2%)	0.678
Hematoma requiring drainage	2 (0.8%)	1 (0.4%)	0.838
Seroma formation requiring drainage	20 (7.8%)	13 (5.1%)	0.415
Transient hypocalcemia	45 (17.6%)	13 (5.1%)	0.006*
Permanent hypocalcemia	0%	1 (0.4%)	0.605
Transient recurrent laryngeal Nerve compromise	29 (11.4%)	3 (1.2%)	0.0001*
Permanent recurrent laryngeal nerve compromise	0	3 (1.2%)	0.202
Recurrence (over a period of at least 6 months–7 years)	2 (0.8%)	0	0.362

Abbreviations: WHO, World Health Organization.

Means and percentages have been counted as appropriate. Mann-Whitney U t-test, Kruskal-Wallis test and Fisher exact test were applied as appropriate to find a significant difference between the groups. A p- value <0.05 was considered statistically significant.

The rate of transient RLN compromise was 11.4% in Group 1 versus 1.2% in Group 2. All three patients with permanent damage of the RLN had significant local factors; two patients had upper pole papillary tumors involving the RLN, while one suffered damage to the medial branch of the RLN during dissection.

Other complications, including operative time, hospital stay, pain scores, analgesia requirement, wound infection, seroma, hemorrhage and recurrence did not differ between the groups.

The subgroup analysis of the patients who presented with complications showed that malignancy and extent of surgery correlated positively with complications when the dissection was performed along the RLN, as summarized in Table 3 . Papillary carcinoma and higher extent of operative dissection in form of total thyroidectomy positively correlated with higher chances of postoperative hypoparathyroidism and RLN compromise; however, considering the sample size of the subgroups, this data should only form a basis for further enquiry on these parameters.

Table 3

Subgroup Analysis of the Patients having Pertinent Complications

Parameter		Transient Hypocalcemia				Transient RLN Compromise				Permanent RLN Compromise				Recurrence
		Group1	Group 2	Pearson chi-squared	p-value	Group1	Group 2	Pearson chi-squared	p-value	Group1	Group 2	Pearson chi-squared	p-value	Group1	Group 2	Pearson chi-squared	p-value
Pathological diagnosis	Benign Follicular Lesion	0 (83)	0 (87)	−	−	12 (83)	1 (87)	10.653	0.001	0 (83)	0 (87)	−	−	1 (83)	0 (87)	1.054	0.488
	Benign Hyperplastic Gland	5 (23)	1 (22)	2.877	0.187	4 (23)	0 (22)	4.199	0.109	0 (23)	0 (22)	−	−	0 (23)	0 (22)	−	−
	Follicular Carcinoma	3 (16)	4 (24)	0.029	1.000	1 (16)	0 (24)	1.538	0.400	0 (16)	1 (24)	0.684	1.00	0 (16)	0 (24)	−	−
	Papillary Carcinoma	35 (126)	8 (116)	19.09	0.000*	11 (126)	2 (116)	6.137	0.047	2 (126)	0 (116)	2.190	0.334	1 (126)	0 (116)	0.965	0.620
	Primary Thyrotoxicosis	2 (9)	0 (12)	1.778	0.475	1 (9)	0 (12)	0.830	1.00	0 (9)	0 (12)	−	−	0 (9)	0 (12)	−	−
Operative Extent	Thyroid Lobectomy	0 (92)	0 (99)	−	−	12 (92)	1 (99)	10.886	0.001*	0 (92)	0 (99)	−	−	0 (92)	0 (99)	1.082	0.482
	Completion Thyroidectomy	4 (8)	2 (13)	2.908	0.146	0 (8)	0 (13)	−	−	0 (8)	0 (13)	−	−	0 (8)	0 (13)	−	−
	Total Thyroidectomy	35 (138)	9 (127)	16.895	0.02*	14 (138)	2 (127)	8.930	0.012*	0 (138)	2 (127)	2.190	0.335	0 (136)	2 (127)	−	−
	Total Thyroidectomy with Neck Dissection	6 (19)	2 (17)	2.038	0.236	3 (19)	0 (17)	2.928	0.231	0 (19)	1 (17)	1.150	0.472	0 (19)	0 (17)	0.920	1.000
Functional Status	Euthyroid	40 (218)	12 (217)	17.624	0.000*	24 (218)	3 (217)	17.732	0.000*	3 (218)	0 (217)	3.035	0.210	2 (218)	0 (217)	2.037	0.361
	Hypothyroid	0 (3)	0 (2)	−	−	1 (3)	0 (2)	0.833	1.000	0 (3)	0 (2)	−	−	0 (3)	0 (2)	−	−
	Hyperthyroid	5 (46)	1 (52)	3.635	0.085	4 (46)	0 (52)	3.558	0.098*	0 (46)	0 (52)	−	−	0 (46)	0 (52)	−	−

The subgroup analysis was performed among various pertinent factors that may influence the complications related to the selection of the plane of dissection. The Pearson chi-squared values, p-levels and Fisher exact test were used as appropriately considering the expected counts. P < 0.05 was considered statistically significant.

Discussion

Preventing RLN injuries and devascularization of parathyroid glands is a technically daunting surgical skill that depends on many factors, including surgeon experience, volume of surgery, and quality of the training of the endocrine surgeon. 8 10 19 Anatomical variations make process of dissection even more challenging. 15 20 The ability of the surgeon to recognize and adapt to anatomical variations remains the most important determinant of overall outcome of the operation. Moreover, fibrosis, adhesions and malignant invasion have their own bequest to add up to this complexity. 21 22

As shown in the present study, the plane of dissection can enormously influence the outcome of the procedure. Many parathyroid glands lie in close association with the thyroid capsule, especially the inferior ones, which may be saved more reliably if dissected along the capsule. 23 Similarly, the incidence of injuries may be intuitively lessened if the dissection is performed along the capsule. The data of the present study corroborates this intuitive notion. In certain circumstances, it may become quite difficult to dissect along the capsule, or the local pathology may dictate the surgeon to dissect along the nerve. Here, the value of intraoperative nerve monitoring comes to focus. 20 24 25

Transient RLN compromise has been traditionally under-reported. Despite a very careful dissection, the incidence of neuropraxia leading to transient RLN compromise remains quite high in our study, of up to 11% if dissected along the nerve, and of ∼ 5% if dissected along the capsule. 26 The nerve injuries are related to traction, cautery, and dissection-related devascularization. No patient in our study exhibited bilateral paralysis. The decision in favor of dissection along the thyroid capsule is straightforward in case of a benign pathology; however, in many instances, the dissection becomes difficult along the capsule, and it may have to be opted to dissect along the nerve.

Inherently, the dissection along the thyroid capsule has many disadvantages. The surgeon may have to rely on the projected course of RLN and would naturally be inclined to leave a small sleeve of thyroid tissue. This loss of clarity about the nerve along the ligament of Berry can put the nerve at higher risk. Moreover, if the surgeon leaves a sleeve of thyroid tissue while saving the nerve, this may lead to inadequate resection, especially when dealing with a malignant gland. Similarly, the tumor involving the upper pole and the ligament of Berry area can be very tricky regardless of the chosen plane of dissection, since, at times, there is complete loss of the planes.

It remains imperative to understand why dissection along the nerve is potentially more harmful for the patient. There can be many plausible explanations, of which one is the devascularization and manipulation of the nerves and of the parathyroid glands during dissection. 26 Other reasons could be the adhesions related to redo surgery, radiation, of fibrosis due to some inflammatory condition like thyroiditis or malignant invasion itself. 17 The subgroup analysis of the present study clearly points towards these plausible reasons.

The present study has many limitations. It is a retrospective analysis, and many factors play a role as the patient develops these complications. The subgroup analysis needs to be interpreted very carefully and would require further confirmation through clinical trials.

Conclusion

In conclusion, dissection along the capsule of the thyroid during thyroidectomy appears to be a safer plane in terms of low complication rate as opposed to dissection along the nerve. It may be employed increasingly, especially for benign pathologies of thyroid gland.