• Users Online: 191
  • Print this page
  • Email this page

 Table of Contents  
Year : 2021  |  Volume : 54  |  Issue : 6  |  Page : 219-225

Does goitre size and delayed surgical intervention adversely affect surgical outcome? A multi-centric experience on thyroidectomy

1 Department of Endocrine Surgery, Baby Memorial Hospital, Kozhikode, Kerala, India
2 Department of Endocrine Surgery, Endocare Hospital, Vijayawada, Andhra Pradesh, India

Date of Submission15-Dec-2020
Date of Decision02-Feb-2021
Date of Acceptance27-Sep-2021
Date of Web Publication30-Nov-2021

Correspondence Address:
Pradeep Puthen Veetil
Department Endocrine, Surgery Baby Memorial Hospital, Kozhikode - 673 004, Kerala
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/fjs.fjs_223_20

Rights and Permissions

Background: Patients with Grade 2 goiters are followed up nonoperatively. Surgical anatomy is altered as nodules/goiter increases to Grade 3. The aim of the study was to analyze the results of thyroidectomy on Grade 2 versus Grade 3 goiter in terms of intra-operative surgical difficulty and surgical outcomes.
Materials and Methods: Multi-centric cross-sectional analytical study. Retrospective analysis of the operative records of the patients undergoing transcervical total thyroidectomy (TT) from 2010 to 2019, satisfying the inclusion and exclusion criteria were included. Based on goiter size, patients were grouped as Group A and B. The important surgical landmarks and surgical outcomes were compared.
Results: Of 2825 cases included, 1697 patients had Grade 2 and 1128 had Grade 3 goiter. In Group A, 1325 underwent TT and 372 underwent hermithyroidectomy (HT). In Group B, 965 had TT and 163 had HT. Group B patients were older and had a longer duration of goiter. In Group A, 3022 recurrent laryngeal nerves (RLN), 3022 external branches of superior laryngeal nerve (EBSLN) and 6044 parathyroid positions, and in Group B, 2093 RLNs, 2093 EBSLNs, and 4186 parathyroid positions were analyzed. Group B had more incidences of “Type C” relationship between RLN and ligament of Berry. EBSLN was Type II in 62% of Group B and 25.5% of Group A. Tubercle of Zuckerkandl was Grade 2/3 in Group B. Group B had longer cervical incisions, more parathyroid auto-transplantation, increased flap edema, seroma, voice change, temporary RLN palsy and hypoparathyroidism.
Conclusion: Early surgery at grade 2 before it progresses to grade 3 goiter appears to have better surgical outcome.

Keywords: Delayed surgery and thyroidectomy outcome, grade of goiter, hypoparathyroidism, recurrent laryngeal nerve

How to cite this article:
Veetil PP, Panchangam RB. Does goitre size and delayed surgical intervention adversely affect surgical outcome? A multi-centric experience on thyroidectomy. Formos J Surg 2021;54:219-25

How to cite this URL:
Veetil PP, Panchangam RB. Does goitre size and delayed surgical intervention adversely affect surgical outcome? A multi-centric experience on thyroidectomy. Formos J Surg [serial online] 2021 [cited 2022 Jan 16];54:219-25. Available from: https://www.e-fjs.org/text.asp?2021/54/6/219/331638

  Introduction Top

Globally, the total goiter prevalence in general population is estimated to be 15.8% and in India at 20.5%. In the United States of America, it is around 4.7% and in Africa 28.3%.[1],[2] Thyroid cancer forms one of the most common malignancies in India. Thyroid cancer constitutes 5.71% of all the cancers in Indian women.[3] Most of the Indian patients who present with goiters are initially evaluated by the physicians. Ultrasound examination (USG) and ultrasound-guided fine-needle aspiration cytology (FNAC) are done to determine the nature of the thyroid nodules based on Thyroid imaging reporting and data system (TIRADS)[4] and Bethesda criteria, respectively.[5] It is then decided whether a patient has to undergo surgery or regular follow-up. TIRADS 4B and above as well as nodule, which is Bethesda IV and above, are referred for surgery; others are advised to undergo periodic follow-up. Once the goiters are deemed to be surgically intervened, the cases are referred to a general or endocrine surgeon.

Nodule growth during follow-up is considered significant only if the volume changes by >50% from the baseline in many studies, but any increase as slight as 10% from baseline is a growth from the patient's perspective.[6] Follow-up has shown that 86.9% of the swelling remain at the same size or grew[6] and only 13.1% show signs of decrease in size even though it does not disappear.[6] With 50% increase in volume as a criterion, 15% nodules show growth.[6] Some studies show that up to 61.2% of the nodules grow on follow-up if growth is defined as 30% increase in volume from baseline.[7] Another study which defined growth as more than 15% increase in volume from baseline show that 89% of the nodules grow on follow-up.[8] Hence, a significant number of patients see that their goiters either remain static or increase in size from Grade 2 to Grade 3.

Often, the goiters are referred for surgery at later stages after long periods of conservative follow-up, when patients experience symptoms such as cosmetic disfigurement due to larger goiters, compressive symptoms, secondary thyrotoxicosis, or even malignant transformation. On the contrary, a goiter primarily evaluated by surgeon, tend to have earlier surgical intervention at smaller sizes, obviating the sequelae of prolonged follow-up. In this context, we set out to analyze our results with thyroidectomy on a Grade 2 versus Grade 3 goiter in terms of intraoperative surgical difficulty and surgical outcomes.

  Materials and Methods Top

Multicentric cross-sectional analytical study conducted at four tertiary care endocrine surgical centers. Institutional ethical committee approval was taken prior to the study (approval number: BMH/IEC/30/2020). Retrospective analysis of the operative records of the patients undergoing transcervical total thyroidectomy (TT)/hemithyroidectomy (HT) from April 2010 to April 2019 satisfying the inclusion and exclusion criteria were included in the study. Patients who underwent surgery for carcinoma thyroid (Stage >T1N0), recurrent goiters, retrosternal goiters needing sternotomy, history of previous neck surgeries, intraoperative findings of thyroiditis and endoscopic thyroidectomies were excluded from the study. Long-term complications data on permanent hypocalcemia/hypoparathyroidism were excluded if the patient did not have a minimum of 1 year follow-up. Cases where operation notes were not maintained and lacked details were excluded. The demographic profile, intra-operative anatomical findings, postoperative morbidity data were assessed. The age, sex, thyroid function, ultrasound findings, FNAC were evaluated. The operative findings and data are entered routinely in separate pro forma maintained in the respective departments [Figure 1]. For purpose of study, the patients who satisfy the inclusion criteria were divided into two groups based on the Grade (WHO criteria) as Grade 1 to Grade 3.[9] Grade 1 goiter is not visible even with neck extension, Grade 2 goiter is seen with neck extension and Grade 3 is seen with neck in neutral position even from a distance. All patients with goiters visiting our outpatient department were graded clinically. In this study, we included Grade 2 (Group A) and Grade 3 (Group B) goiters. Apart from this, for the purpose of analysis, the patients who had gland weight <75 g were included in Grade 2 (Group A) and >75 g in Grade 3 (Group B). The weight varied between 45 and 75 g in Grade 2 and between 76 and 424 g in Grade 3. [Figure 2] shows a few of the Grade 3 goiters (preoperative and intraoperative images). The most common complications of thyroid surgery are voice changes (External and recurrent laryngeal nerve injuries; EBSLN and RLN) and hypoparathyroidism. The extent of handling of the RLN can determine the occurrence of neuropraxia or permanent damage. This, in turn, depends on certain anatomical relations of the RLN such us Ligament of Berry (L of B), Tubercle of Zuckerkandl (T of Z), and branching patterns of the RLN. These parameters are compared between Group A and Group B. The Grading of T of Z and the classification of EBSLN is shown in [Table 1].[10],[11] The relationship of the terminal portion of RLN before entering the larynx to the L of B is shown in [Table 1].[10] The position of parathyroids observed during the thyroidectomy is described as given in [Table 2].[11] The position of superior and inferior parathyroids are depicted in [Figure 3]. The length of the incision, the need to divide strap muscles for safe transcervical thyroidectomy, and the need for parathyroid auto-transplantation are also compared between Groups. Postoperatively, patients undergo indirect laryngoscopy before discharge or after 6 weeks. Serum calcium estimation is performed at 24 h after thyroidectomy and prior to discharge. The postoperative complications such as wound infection, flap edema, voice change without laryngeal nerve palsy, RLN palsy (temporary/permanent), and hypocalcemia (temporary/permanent) are compared between groups A and B. Permanent hypocalcemia and permanent hypoparathyroidism are defined as lasting for more than 6 months after thyroidectomy. This study complied with the international ethical norms of the Helsinki Declaration – Ethical Principles for Medical Research Involving Human Subjects, 2013.[12] Informed consent was obtained from all the patients involved in the study.
Figure 1: The operation notes entry Form

Click here to view
Figure 2: Grade 3 goiter: Preoperative and intraoperative images

Click here to view
Table 1: Description of external branches of superior laryngeal nerve, Ligament of Berry and Tubercle of Zuckerkandl

Click here to view
Table 2: Descriptive anatomic location of parathyroids[11]

Click here to view
Figure 3: Depicts the positions of the superior and inferior parathyroids in relation to thyroid. Pictorial representation of the locations of superior and inferior parathyroid [Table 2] Locations: Superior parathyroid A Type 1, B Type 2, C Type 3 Inferior Parathyroid: D Type 1, E Type 2, F Type 3 Other Landmarks: G: Recurrent laryngeal Nerve, H Thyroid gland, I: Larynx, J: Hypoid, K: Thymic Limb

Click here to view

Statistical analysis was done with SPSS 20 version, IBM, USA. Descriptive analysis, t-test, Chi-square tests were employed.

  Results Top

A total of 4896 patients underwent thyroid surgery. After exclusion criteria were applied, 2825 cases were included. There were 1697 patients with grade 2 goiter (Group A) and 1128 patients with Grade 3 goiter (Group B). In Group A, 1325 patients had TT and 372 patients had HT. In Group B, 965 patients had TT and 163 patients had HT. The patients who had Grade 3 goiters were older in age and had longer duration of goiter [Table 3]. In Group A (which included 1325 TT + 372 HT), 3022 RLN, 3022 EBSLN and 6044 parathyroid positions and in Group B (965 TT and 163 HT), 2093 EBSLN, 2093 RLN, and 4186 parathyroid positions were analyzed. [Table 3] depicts the relationship of the terminal portion of RLN with L of B, types of EBSLN and the Grades of T of Z seen in the two groups. Patients with Grade 3 goiter (Group B) had significantly more incidence of “Type C” relationship between RLN and L of B. EBSLN was Type II A or B in 62% of the patients in Group B and 25.5% of patients in Group A. T of Z was observed to be Grade 2/3 in significantly more number of patients in Group B. T of Z is well known to change the position of the RLN and the superior parathyroids. The number of parathyroids auto-transplanted was higher in Group B [Table 3]. The inferior parathyroid position was significantly altered in Grade 3 goiters making them at risk of devascularization [Table 4]. The superior parathyroid positions were comparable among the two groups.
Table 3: Demographic profile and intra-operative anatomy

Click here to view
Table 4: Comparison of the intraoperative parathyroid locations in both the groups

Click here to view

The cervical incision was longer in Group B, and they also had more incidences of flap edema and seroma which needed aspiration [Table 5]. Voice change unrelated to RLN injury was seen more in group B [Table 5]. Incidence of temporary RLN palsy and hypoparathyroidism was significantly more in Group B; however, there was no significant difference in permanent RLN palsy or hypoparathyroidism between the groups. RLN branching did not differ between the groups. The incidence of hemorrhage and tracheomalacia (3/1128 in Group B) were not significantly different between groups. The case referral pattern revealed that among patients in Group A, 65% (n = 1103) cases were directly consulted by the surgeon; whereas in Group B, 81% (n = 914) of the patients were referred to the surgeon by physicians. This frequency difference was statistically significant (P = 0.009).
Table 5: Postoperative complications

Click here to view

  Discussion Top

In clinical practice, detection of thyroid nodules has become very common in India. With widespread use of ultrasound, the detection of thyroid nodules is 19%–68% of the screened persons.[13] There are well laid down guidelines on how these nodules have to be investigated.[13] Once the initial assessment with imaging and FNAC is done, nodules which need surgical removal as per guidelines is referred to surgeons. The psychological stress in patients who do not satisfy the guidelines for surgical intervention remain an issue since they have approached the clinician for definitive treatment of nodules. Since considerable number of patients on conservative follow-up show growth in nodule size (depending on the definitions of growth),[6],[7],[8] it becomes important that the surgical outcomes of operating a large goiter versus a small goiter be explained to the patients during initial counseling on the management options. Studies on natural disease history show that the growth of nodules was found in up to 89% of cases.[8] Even meta-analytical studies show, only 10%–17% of nodular goiters regress with nonoperative thyroxine suppression therapy.[14],[15] Only one meta-analysis reported goiter regression in 50% of cases, but this response was observed in highly selected group of young patients with small euthyroid goiters and no comorbidities.[16]

Various studies have shown that thyroidectomy results in very few complications in experienced surgical hands.[17],[18] However, even with experienced surgeons, morbidity does happen, especially with large Grade 3 and substernal goiters.[19],[20] In this study, two surgeons trained in endocrine surgery performed the operations at four tertiary care centers. Our results show that outcomes in larger Grade 3 goiters are different even though the same surgeons performed all the cases irrespective of the grade of the goiter. The aim of this study is to analyze the outcomes between Grade 2 and Grade 3 goiters since many patients are now referred for surgery only when the goiters show considerable growth during the follow-up.

Grade 3 patients who undergo transcervical thyroidectomy needs larger incisions and consequently have a higher incidence of flap edema. Grade 3 goiters also have higher incidence of seroma which need aspiration at least once, and can be attributed to larger dead space after the thyroidectomy. In Indian patients, presence of flap edema and seroma delay the discharge and prolong duration of hospital stay. On comparing the two groups, the intraoperative findings show that the relationship of the terminal portion of RLN to the L of B is of “Type C” in significantly more number of patients, which means the surgeon will have to dissect through L of B to release the nerves. This can result in RLN injury, bleeding from L of B, resulting in electrocautery use. Significantly more patients of Group B had Grade 2 and 3 T of Z, which is well known to alter the course of RLN, necessitating more dissection to free the RLN. In Group B, temporary RLN palsy was significantly higher than Group A (P = 0.001). This could be due to the unfavorable and difficult RLN course with respect to L of B. T of Z can become an issue in thyroid surgery, especially with inexperienced surgeons.[21] Patients in Group B had voice changes without any evidence of RLN palsy (P = 0.003), which could be EBSLN related or due to division of strap muscles performed during thyroidectomy for majority of Grade 3 goiters.

Our data also showed that the incidence of temporary hypoparathyroidism was significantly higher in Group B (P = 0.01). We also found that more parathyroids were at risk of iatrogenic injury due to Type 1 location of inferior parathyroids. This necessitated more number of parathyroids to be auto transplanted in Group B (P < 0.0001). Larger goiter size did not produce a significant change in superior parathyroid location unlike the inferior parathyroids.

It was also noted that EBSLN was Type 1 in 61.8% of Group A patients, but it was Type II in 62% of Group B patients. Type II location predisposes EBSLN injury since it has to be dissected off the thyroid pole and may result in neuropraxia. It is well documented in literature about the higher incidence of Type 2 EBSLN with Grade 3 goiter.[22],[23] On analyzing the referral pattern, it was seen that most of the patients with Grade 2 goiters had consulted the surgeons directly and had early surgery, whereas >80% of the patients with Grade 3 goiters had consulted physicians initially and were referred to surgeons due to growth of the nodules after variable follow-up periods. This showed a treatment bias based on whether the patients consulted the surgeon or physician initially.

The apparent strengths of this study are large cohort with complete data, multi-center experience, comparison of parameters between Grade 2 and grade 3 goiters, comprehensive analysis of surgical aspects, and one of a kind study from the Indian subcontinent. The few shortcomings in this study are retrospective design and extrapolative (based on personal experience and literature) assumption that most of the Grade 2 goiters will progress to Grade 3. Although we have not directly compared our results with any conservatively treated cohort, the significant difference between frequencies of cases referred by physicians for surgery was inversely proportional to respective frequencies of surgical morbidity in Grade 2 and 3 goiters. We opine that these observations act as an indication to operate the goiters, before they grow to Grade 3. We also agree that a randomized controlled trial involving Grade 2 and 3 goiters with a prospective study design would be an ideal method to study the outcomes, which can be carried out by centers involved in large scale thyroid surgeries.

  Conclusions Top

Patients with Grade 3 goiters need longer incisions, have a higher incidence of flap edema, seroma, postoperative voice change, temporary hypocalcemia, and temporary RLN palsy. They also need strap muscle division and many need parathyroid auto-transplantation. Hence, when follow-up option in goiter management is discussed with the patient, the surgical aspects which make Grade 3 goiter slightly risky when compared to surgery on Grade 2 goiter should also be discussed. This may result in more patients opting for earlier surgical intervention before Grade 2 goiter increases to Grade 3, resulting in prevention of morbidities and facilitating safe thyroidectomy. This study also gives an occult message, that Grade 3 goiters are better managed by an experienced endocrine surgeon than a surgeon performing thyroidectomy occasionally. At present, we do not feel that, due to these surgical difficulties observed in Grade 3 goiter even in experienced hands, one should prompt surgery for Grade 2 goiters. However, we do hypothesize that patients should be given the option of earlier surgical intervention based on risks of surgery at later stages and that there is a need to consider this option while framing future guidelines for the management of thyroid nodules. More studies, preferably prospective randomized trials from multiple centers, are needed to establish these hypotheses.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

Mesele M, Degu G, Gebrehiwot H. Prevalence and associated factors of goitre among rural children in Northwest Ethiopia, cross sectional study. BMC Public Health 2014;14:130. Available from: http://www.biomedcentral.com/1471-2458/14/130. [Last accessed on 2020 Oct 25].  Back to cited text no. 1
Kalra S, Unnikrishnan AG, Sahay R. The global burden of thyroid disease. Thyroid Res Pract 2013;10:89-90. doi: 10.4103/0973-0354.116129.  Back to cited text no. 2
  [Full text]  
Unnikrishnan AG, Menon UV. Thyroid disorders in India: An epidemiological perspective. Indian J Endocrinol Metab 2011;15:S78-81.  Back to cited text no. 3
Tessler FN, Middleton WD, Grant EG. Thyroid imaging reporting and data system (TIRADS): A users guide. Radiology 2018;287:29-36. doi: 10.1148/radiol. 2017171240.  Back to cited text no. 4
Cibas ES, Ali SZ. The Bethesda system for reporting thyroid cytology. Am J Clin Pathol 2009;132:658-65. doi: 10.1309/AJCPPHLWMI3JV4LA.  Back to cited text no. 5
Durante C, Costante G, Lucisano G, Bruno R, Meringolo D, Paciaroni A, et al. The natural history of benign thyroid nodules. JAMA 2015;313:926-35.  Back to cited text no. 6
Quadbeck B, Pruellage J, Roggenbuck U, Hirche H, Janssen OE, Mann K, et al. Long-term follow-up of thyroid nodule growth. Exp Clin Endocrinol Diabetes 2002;110:348-54.  Back to cited text no. 7
Alexander EK, Hurwitz S, Heering JP, Benson CB, Frates MC, Doubilet PM, et al. Natural history of benign solid and cystic thyroid nodules. Ann Intern Med 2003;138:315-8.  Back to cited text no. 8
Peterson S, Sanga S, Eklof H, Bunga B, Taube A, Gebre-Medhin M, et al. Classification of thyroid size by palpation and ultrasonography in field surveys. Lancet 2000;355:106-10. doi: 10.1016/s0140-6736 (99) 07221-9.  Back to cited text no. 9
Pradeep PV, Jayashree B, Harshita SS. A closer look at laryngeal nerves during thyroid surgery: A descriptive study of 584 nerves. Anat Res Int 2012;2012:490390.  Back to cited text no. 10
Pradeep PV. A closer look at parathyroid anatomy during thyroid surgery. BMH Med J 2014;1:66-71.  Back to cited text no. 11
World Medical Association. World medical association declaration of Helsinki: Ethical principles for medical research involving human subjects. JAMA 2013;310:2191-4. doi: 10.1001/jama. 2013.281053.  Back to cited text no. 12
Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, et al. 2015 American Thyroid Association Management Guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: The American Thyroid Association Guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid 2016;26:1-133.  Back to cited text no. 13
Zelmanovitz F, Genro S, Gross JL. Suppressive therapy with levothyroxine for solitary thyroid nodules: A double-blind controlled clinical study and cumulative meta-analyses. J Clin Endocrinol Metab 1998;3:3881-5.  Back to cited text no. 14
Castro MR, Caraballo PJ, Morris JC. Effectiveness of thyroid hormone suppressive therapy in benign solitary thyroid nodules: A meta-analysis. J Clin Endocrinol Metab 2002;87:4154-9.  Back to cited text no. 15
Yousef A, Clark J, Doi SA. Thyroxine suppression therapy for benign, no n-functioning solitary thyroid nodules: A quality-effects meta-analysis. Clin Med Res 2010;8:150-8.  Back to cited text no. 16
Zambudio AR, Rodríguez J, Riquelme J, Soria T, Canteras M, Parrilla P. Prospective study of postoperative complications after total thyroidectomy for multinodular goiters by surgeons with experience in endocrine surgery. Ann Surg 2004;240:18-25.  Back to cited text no. 17
Stavrakia AI, Ituarte PH, Ko CY, Yeh MW. Surgeon volume as a predictor of outcomes in inpatient and outpatient endocrine surgery. Surgery 2007;142:887-99.  Back to cited text no. 18
Abbas A, Sakkary M, Naser A. Challenges for huge goitre surgery. Egypt J Surg 2019;38:338-47. doi: 10.4103/ejs.ejs_212_18.  Back to cited text no. 19
  [Full text]  
Pradeep PV, Sattar V, Krishnachaithanya K, Ragavan M. Huge thyromegaly: Challenges in the management. ANZ J Surg 2011;81:398-400.  Back to cited text no. 20
Chintamani. “Friend or Foe” of a Thyroid surgeon?-The tubercle of zuckerkandl. Indian J Surg 2013;75:337-8.  Back to cited text no. 21
Potenza AS, Araujo Filho VJ, Cernea CR. Injury of the external branch of the superior laryngeal nerve in thyroid surgery. Gland Surg 2017;6:552-62.  Back to cited text no. 22
Ravikumar K, Sadacharan D, Muthukumar S, Mohanpriya G, Hussain Z, Suresh RV. EBSLN and factors influencing its identification and its safety in patients undergoing total thyroidectomy: A study of 456 cases. World J Surg 2016;40:545-50.  Back to cited text no. 23


  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

  In this article
Materials and Me...
Article Figures
Article Tables

 Article Access Statistics
    PDF Downloaded152    
    Comments [Add]    

Recommend this journal