INTRODUCTION:

The utmost common problems conversed with patients who experience thyroid surgery are hemorrhage, recurrent or external laryngeal nerve paralysis, hypocalcemia and hypoparathyroidism. However, injury of the external branch of superior laryngeal nerve (EBSLN) may happen through the ligation of the superior thyroid artery in about 58% of patients, and its revealing post operatively is hampered by the variable and restrained signs and alterations on post-operative laryngoscopy (1). EBSLN damage lead to prarlysis of the crico-thyroid muscle, which results in change essential occurrence of the voice, a worsening in voice presentation in making high-frequency sounds, and decrease vocal projection. This can be mainly important for those using their voice workwise, for example lawyers, teachers, are considerably at risk by the subtle alterations associated to its injury instead, the insight of an abnormal voice change the quality of life and decrease the over-all health through many methods and patients cannt shout. From that viewpoint, EBSLN injury considers a threat to handicap all patients experiencing thyroid surgery. EBSLN damage can be tough to recognize intra-operatively and is hard to notice through post-operative laryngoscopy (2). The superior laryngeal nerve is one a branch of the vagus nerve (3). The superior laryngeal nerve (SLN) divides into an internal and external branch. The EBSLN run down dorsal to the carotid sheath, and then cross medially, spreading to the larynx. In its passageway, the EBSLN is usually positioned dorsal to the superior thyroid artery and superficial to the inferior pharyngeal constrictor muscle as it run down and crossing medially to innervate the crico-thyroid muscle on the anterolateral part of the lower portion of the cricoid cartilage of the larynx to endorse strength of the vocal fold, thus amassed voice pitch. The close correlation with the superior thyroid vessels (STV) puts the EBSLN in danger each time the superior end of the thyroid is dissected (2,3). Afterward the EBSLN journeys down the lateral surface of the larynx on the lower pharyngeal constrictor muscle, the EBSLN typically splitting into two divisions at the level of the cricoid, entering independently at the par's recta and pars obliqua of the crico-thyroid muscle bellies. The danger of damage to the nerve by transection, traction, entrapment, thermal harm or interrupted blood supply. The possibilities of surgical harm are also amplified by size and weight of the specimen, and little neck length. Cricothyroid muscle electroneuromyography (EMG) is the most exact tool to identify unusual EBSLN conductivity, but it is officially hard and not appropriate in routine preparation. The EBSLN is often about 0.8 mm wide, and its total length varies between 8 and 8.9 cm(4)^.The most largely known surgical cataloging of the EBSLN was planned in 1992 by Cernea et al. (5). In 1998, Kierner et al. put out a similar ordering to the Cernea system, using a fourth features of the EBSLN passing dorsally to the upper thyroid pedicle, which was detected in 13% of their dissection studies and was well-thought-out more difficult to visually identify (3). Numerous methods have been designated to reduce the likely risk of damage to the EBSLN during upper thyroid vessels dissection and ligation:

1. Save ligation of the single divisions of the superior thyroid vessels beneath direct vision on the thyroid capsule without visual identification of the nerve (6).

2. Visual identification of the nerve earlier to ligation of the superior thyroid pole vessels (7).

3. The use of intra operative nerve stimulator or neuro-monitoring for mapping and confirmation of the EBSLN identification (2,5,8, 9-11)

However, many surgeons do not apply this principle to the ESLN, and hence we conducted this study to assess the rate of ESLN injury during thyroidectomy when segregation of superior thyroid vessels and then ligated individually in branches very close to thyroid gland capsule without nerve stimulator or intraoperative neuro-monitoring.

PATIRNTS AND METHODS:

The present study is a prospective, non- randomized clinical study included 1450 patients underwent either (total thyroidectomies, near total thyroidectomies or lobectomy and isthmectomy) in the Surgical Department/AL-Diawaniyah Teaching Hospital in Diawaniyah City, between January 2000 and February 2018 . Preoperative workup included full history taking, general and local clinical examination, and routine laboratory investigations in addition to thyroid function tests and serum calcium level, and neck ultrasonography. Fine needle aspiration cytology was performed on selected basis (suspicious lesions). Preoperative normalization of thyroid hormones and serum calcium levels. Exclusion criteria were previous neck irradiation, previous laryngeal or thyroid surgery or any other cervical exploration, vocal cord disorders, preoperative voice changes, and those with thyroid malignancy with extra thyroid extension were excluded from the study. All patients underwent a detailed voice evaluation was typically performed by fibroptic laryngoscopy for sub-clinical vocal cord paralysis, comprising faintness after use, incapability to reach high pitch or alteration in essential talking regularity. Pre-operatively, the sign of EBSLN damage on laryngoscopy were taken as rotation of posterior glottis near side of the damaged and bowing and displacement of affected vocal cord.

Operative technique was constructed to evade surgical bias. Surgeries were done by training level of the senior surgeon only. In case of patient had a over-all thyroidectomy, all sideways of the organ was well-thought-out as single unit. Thyroid was uncovered after removing of platysma flap superiorly and inferiorly through a low transverse collar incision at the lower neck. The strap muscles were separated to expose the goiter. Subsequent to suturing of middle thyroid vein and entire medial rotation of lobe, superior end planning was begun. Care should be taken and stay near to capsule of organ and dissecting both laterally and at the fusion of upper thyroid pole with upper border of isthmus, the whole pole was encircled and taped. With gentle traction on this tape, additionally enabled by using of a hemostat at lateral edge of the pole. Watchful dissection in avascular crico-thyroid space was then initiated and care was taken to recognize nerve in this space. Capsular dissection, skeletonization and single ligation of superior polar vessels were then done. Keeping crico-thyroid muscles intact was emphasized during dissection. Integrity of strap muscles was restored if muscle cutting was performed. Closed negative suction drain was utilized routinely for every patient in the study.

All patients underwent follow-up for detailed voice evaluation was typically performed by fibroptic laryngoscopy for sub-clinical vocal cord paralysis on the 7^th postoperative day. And long term follow-up of patients was carried out through physical examinations clinical history and conducted with each subsequent clinic visit .The transit EBSLN injury mean the voice retain to normal between a period of (3wk-3month).Outpatient and telephone visit follow-up examinations were performed for all patients ranging from 7 days, 1 month, 3month, 6 months, 9month , 1year to 17years after operation for the assessment of complications and the mean of 10 years interval. Therefore, telephone visits were particularly useful in the long-term. Patients with voice changes, suspected nerve injury, and those with hypocalcemia were followed up every month at any time during their postoperative course for the detection of any improvement and better evaluation of their conditions .The patient were included in presented study, categorized in to the following as show in table (1) .

Table (1): - characteristic of patients study preoperatively.

Patients characteristics (total n=1450)	Number/percentage
Sex of patients
Male	160 (11%)
Female	1290 (89%)
Age of patients
(range)	25y -70y
Mean ± SD	40±10
Type of operation
Total thyroidectomy	376 (25.9%)
Near total thyroidectomy	472 (32.6%)
Lobectomy and isthmusectomy	602 (41.5%)
Thyroid disease
Solitary nodule of multinodular goiter	465 (32%)
Multinodular goiter	900 (62.1%)
Diffused goiter	85 (5.9%)
Size of goiter
Small goiter	930 (64.1%)
Large goiter	520 ( 35.9%)
Disease of thyroid
Benign lesion	1130 (77.9%)
Malignant	320 (22.1%)
Follow up	At 7day, 1mth, 3mth, 6mth , 9mth , 1-17year

All patients were included in presented study signed an informed consent form, for operation and well explain the possible complication and this approved by the Ethics Committee of the Medical Research institute.

Statistical analysis: - SPSS version 16 and Microsoft Office Excel 2007, Chi-square test and Fisher exact test all used to study association between any two nominal variables. P-value of less than or equal to 0.05 was considered significant.

RESULTS:

In the present study, post-operative data of the studied group are shown in Table (2). The total number of patients 1450 underwent thyroidectomy, in which EBSLN injury 38 (2.6%) ,include transient injury 28 (1.9%), whereas permanent injury occurred in 10 (0.7%) patients .The EBSLN injury in 22(1.5%) in total thyroidectomy, 4(0.3%) occur in near total thyroidectomy whereas 12 (0.8%) occur in lobectomy and isthmusectomy . EBSLN injury occur 25(1.7%) in male whereas in female 13(0.9%). Majority of EBSLN injury occur in large goiter 29(2%) whereas in small goiter occur in 9(0.6%). in addition to these data EBSLN injury occur in teacher 3(0.2%), in orator 2(0.1%) whereas 33(2.3%) work others job. As shown in table (2).

Table (2):- Postoperative ESLN assessment of studies patients (total number of cases =1450)

ESLN assessment	Number/ percentage
EBSLN intact	1412 (97.4%)
EBSLN injury	38 (2.6%)
ESLN injury
Transient injury	28 (1.9%)
Permanent injury	10 (0.7%)
Type of surgery
Total thyroidectomy	22 (1.5%)
Near total thyroidectomy	4 (0.3%)
Lobectomy and isthmusectomy	12 (0.8%)
According to sex
Male	25 (1.7%)
Female	13 (0.9%)
According to size of goiter
Large goiter	29 (2%)
Small goiter	9 (0.6%)
According to job
Teacher	3 (0.2%)
Orator	2 (0.1%)
Others	33 (2.3%)

The most common complication post-operative thyroidectomy which caused by EBSLN injury in study groups, loss of high pitch voice 11(0.7%), Chocking 8(0.6%) whereas both loss of high pitch voice and Chocking 19(1.3%). As shown in table (3).

Table (3):-Post-operative EBSLN injury in the study groups .

Complication of ESLN injury
Loss of high pitch voice	11 (0.7%)
Chocking	8 (0.6%)
Both loss of high pitch voice and Chocking	19 (1.3%)

Further postoperative complication of thyroidectomy in studies patients 16(1.1%) tension hematoma, and RLN 18 (1.2%), in which transient injury of RLN 14(1%) whereas permanent injury of RLN 3(0.2%). Transient hypocalcaemia 49(3.4%), permanent hypocalcaemia 3(0.2%), hypothyroidism, thyrotoxic crisis 3(0.2%) whereas wound infection and stick granuloma occur in 32(2.2%) . As shown in table (4).

Table (4) :- Further postoperative complication of thyroid surgery of studies patients (185 patients out 1450 of total cases ) .

Postoperative complication	Number/percentage 185/1450
Tension hematoma	16 (1.1%)
Recurrent laryngeal nerve injury (RLN)	18 (1.2%)
Transient injury of RLN	14 (1%)
Permanent injury of RLN	4 (0.2%)
Hypocalcaemia	52 (3.6%)
Transient hypocalcaemia	49 (3.4%)
Permanent hypocalcaemia	3 (0.2%)
Hypothyroidism	64 (4.4%)
Thyrotoxic crisis	3 (0.2%)
Wound infection and stick granuloma	32 (2.2%
Total number	185 (12.7%)

Correlation between EBSLN injuries with type of operation of patients

In present study the EBSLN injury in total thyroidectomy more than in near total thyroidectomy. Lobectomy and isthmusectomy more than near total thyroidectomy. And these differences was statistically significant differences, (P˂0.005) .As shown in table 5.

Table (5):-EBSLN injury according to type of operation

Type of operation	N/%	P1	P2	P3
Total thyroidectomy	22(1.5%)
Near total thyroidectomy	4(0.3%)	<0.001	0.003	<0.001
Lobectomy and isthmusectomy	12(0.8%)

Correlation between EBSLN injuries with age of patient's study.

In present study there was no significant association between EBSLN injury and type of operation with age of patients, (P>0.005), as shown in the table (6).

Table (6):- Comparison between EBSLN injuries accords to type of operation with age of patients study.

Type of operation	Mean ±SD	P1	P2	P3
Total thyroidectomy	40±9.2
Near total thyroidectomy	40±10	˃ 0.005	˃0.005	˃ 0.005
Lobectomy and isthmusectomy	40±9.5

Correlation between EBSLN injury with sex of patient's study.

In present study the correlation of EBSLN injury and type of operation with male 25 (1.7%) more than in female patients 13 (0.9%) and these differences was statistically significant differences, (P˂0.005) , as shown in the table (7) .

Correlation between EBSLN injuries with size of goiter

In present study the EBSLN injury according to type of operation with large size goiter 29(2%) more than in small size goiter 9 (0.6%) and these differences was statically significant differences, (P˂0.005) , as shown in the table ( 8 ) .

Majority of cases with EBSLN injury were complain from both loss of high pitch voice and Chocking 19 (1.3%) more than loss of high pitch voice 11 (0.7%) and chocking 8(0.6%) and these differences was statistically significant differences, (P˂0.005).

DISCUSSION:

In present study, a large cohort project involving 1450 patients underwent thyroid surgery by using lateralization and segregated ligation of the superior thyroid vessels to minimize the EBSLN injury, without visual identification of EBSLN and without nerve stimulator or intraoperative neuromonitoring .In addition to , long-term follow-up patients which started from 7days after operation (1month , 3month , 6month ,9month ,1year until to 17 year ) was carried out through clinical history and physical examination with each subsequent clinic visit and in addition to post-operative endoscopic examination of the vocal .The total cases with EBSLN injury were 38 (2.6%) , in which the transient EBSLN injury occurred in 28 (1.9%) of patients and permanent injury occurred in 10 (0.7%) of patients .The outcome followed analyzing this large number of cases is promising and reflect the experience of the surgeon.

Large multinodular goiter is one of the main indications for surgery and a risk factor for injury at the same time. In the present study the total cases with large goiter 520 ( 35.9%) and the majority of cases with EBSLN injury were occur in patients with large size goiter 29 (2%) more than small size goiter 9 (0.6%) with statistically significant difference (P ˂0.005) .if the goiter is large, the superior pole occupies a higher position in the neck and is more closely related to the EBSLN in its descending course. Majority of cases with EBSLN injury were occur in male {25(1.7%)} more than female patients {13(0.9%)}, propose that could be the main major cause was the anatomy in male more difficult than the anatomy of female .In addition to these results there was no statistically significant correlation between age of patients and EBSLN injury .Thus, the age of patients can- not play any role in injury of EBSLN .

The results of present study were similar to other results reported by many authors, which used in their studies the same surgical protocol for management of the EBSLN during thyroidectomy as in the present study like Ahmed et al (12), whom reported that the transient EBSLN injury occurred in six (3%) patients, whereas permanent injury occurred in four (2%) patients.

Lekacos et al. (13) whom reported that, 0% EBSLN injury with distal ligation close to thyroid capsule and 5.6% injury with high ligation. Evaluation of EBSLN injury in their study was carried out using indirect laryngoscopy.

And the other studies were reported by, Likewise, Loré et al. (14) and Kierner et al. (3), whom reported that gentle mobilization of upper thyroid pole and individual ligation of superior thyroid vessels very close to thyroid capsule without systematic positive search for the EBSLN may avoid nerve injury.

Whereas other studies, that used the same surgical protocol for management of the EBSLN during thyroidectomy as in the present study, the rate of EBSLN injury was much higher from the presented study and these studies which reported by Aluffi et al. (15) , in which the results were 14% incidence for EBSLN injury despite their small study population (45 patients) and another study which reported by Teitelbaum and Wenig (1) in which the results were, a high permanent nerve injury (5%) . The high rate of EBSLN injury in these two studies may be attributed to the use of both laryngoscopy and electromyography of cricothyroid muscles for the diagnosis of EBSLN injury, whereas, in the present study, we used indirect laryngoscopy post- operative and long-term follow-up through physical examination and clinical history.

On the other hand, the other studies used visual identification of nerve which additional step to their surgical operation protocol i.e (lateralization , visual identification of nerve and individual ligation of superior thyroid vessels ) that studies employ comparative study between visual nerve identification group and non- visual nerve identification group, that found no benefit of systematic search for the EBSLN and these studies which reported by Page et al. (16), and another study which reported by the Bellantone et al. (6) .

Whereas the study that reported by Hurtado-Lopez et al. (17) found that patients who underwent thyroidectomies without searching for the EBSLN had more voice changes compared with patients with thyroidectomies with intentional searching for the nerve (14 versus 8%, respectively) and give emphasis to the importance of intraoperative identification.

While study which reported by Patnaik et al. (18) whom not used comparative study but evaluate the visual identification rate of the EBSLN during 64 thyroidectomies. The nerve was identified and preserved in 83% of patients and could not be identified at all in the remaining patients (17%). None of these patients (17%) showed any symptoms and signs of ESLN paresis as their nerves were preserved using individual ligation of superior thyroid vessels close to thyroid capsule.

In present study, using lateralization and segregated ligation of the superior thyroid vessels to minimize the EBSLN injury, without visual identification of EBSLN and without nerve stimulator or intraoperative neuromonitoring because of some variant anatomy of EBSLN was buried under inferior constrictor muscle fibers, and later on it was impossible to identify the nerve in the field of thyroidectomy. They concluded that trial of nerve identification if it is buried under inferior constrictor muscle fibers would take a longer period of time with more injury to surrounding structures and without any benefit as the nerve could be preserved with individual ligation of superior thyroid vessels close to thyroid capsule. The long-term follow up patients postoperatively through physical examination and clinical history for integrity of vocal cord because of EBSLN injury can be difficult to identify intra-operatively and is difficult to detect during routine postoperative laryngoscopy.

However, other studies which reported by Barczyński et al. (8), Lifante JC (10) and Dionigi G (9), whom used more advance technique for visualization of EBSLN intra-operatively neuromonitoring (IONM) during thyroidectomy ,these study concluded that the use of intraoperative neuromonitoring significantly improved intraoperative identification of the EBSLN and decreased early postoperative voice changes with no significant difference in delayed postoperative voice changes between IONM and surgical visualization. Improvement in the identification rate of the EBSLN by the use of IONM and thus limitation of the risk for nerve. We suggest that despite the benefit of IONM during thyroidectomy in these studies, it could not be used routinely our countries because of deficiency of incomes.

CONCLUSION:

Segregated ligation of superior thyroid artery closely to thyroid capsule without nerve stimulator or intraoperative neuromonitoring is safe technique, cost effective with time preservation but need surgical skill to decrease risk of injury to the external branch of superior laryngeal nerve.

CONFLICT OF INTEREST:

The authors declare no conflict of interests.

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Received on 05.06.2020 Modified on 20.06.2020

Research J. Pharm. and Tech. 2020; 13(7): 3419-3424.

DOI: 10.5958/0974-360X.2020.00608.3

Type of operation	Male	Female	P1	P2	P3
Total thyroidectomy	14(0.9%)	8
Near total thyroidectomy	4(0.3%)	2	˂ 0.005	˂0.005	˂ 0.005
Lobectomy and isthmusectomy	7(0.5%)	3
Total cases	25(1.7%)	13 (0.9%)

Type of operation	Large goiter	Small goiter	P1	P2	P3
Total thyroidectomy	154(1%)	4(0.3%)
Near total thyroidectomy	6(4%)	2(0.1%)	˃ 0.005	˃ 0.005	˃ 0.005
Lobectomy and isthmusectomy	8(0.5%)	3(0.2%)
Total cases	29(2%)	9((0.6%)