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ORIGINAL ARTICLE
Year : 2015  |  Volume : 28  |  Issue : 4  |  Page : 807-812

Parathyroid gland injuries during total and subtotal thyroidectomy


1 Department of General Surgery, Faculty of Medicine, Menoufia University, Zagazig, Sharkia, Egypt
2 Resident of General Surgery at Ministry of Health, Zagazig, Sharkia, Egypt

Date of Submission28-Oct-2014
Date of Acceptance06-Jan-2015
Date of Web Publication12-Jan-2016

Correspondence Address:
Yaser A Saleh
Zagazig
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-2098.173595

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  Abstract 

Objective
The aim of this study was to identify the incidence, risk factors and the clinical relevance of incidental parathyroid excision during total and subtotal thyroidectomy in thyroid diseases.
Background
Postoperative hypocalcaemia is observed in total thyroidectomy patients and it is the most common complication. It is usually transient, and the incidence of permanent hyperparathyroidism is 3% or less. Despite being self-limiting in most patients, symptomatic hypocalcaemia is of particular concern because of a delay in its manifestation and the consequent need for prolonged patient hospitalization or readmission.
Patients and methods
In this randomized prospective study, we surveyed 30 patients who were admitted in the General Surgery Department, Menoufia University Hospital, during the period from November 2012 to March 2014 with benign thyroid diseases such as simple multinodular goiter, secondary toxic goiter, diffuse toxic goiter relapsing after full medical treatment, selected cases of thyroiditis (Hashimoto's thyroiditis) and thyroid cancer.
Results
We found two cases with temporary hypocalcaemia with multinodular goiter and medullary carcinoma. The typical signs and symptoms associated with hypocalcaemia are neuromuscular irritability, including perioral or acral paresthesia, muscle cramps that may progress to carpopedal spasm, laryngospasm, bronchospasm or even tetany. Treatment is based on the severity of symptoms. In severe cases (calcium levels less than 7.5% or severe symptoms), intravenous calcium salts are administered using one ampoule of calcium gluconate in 1 l of 5% dextrose at an initial infusion rate of 100 ml/h. With frequent monitoring of the serum calcium level (usually every 1-2 h), the infusion rate is titrated to keep the serum calcium level in the low normal range.
Conclusion
Incidental parathyroid excision during thyroid resection is not uncommon, and it occurred in 16.4% of the cases in this series. Total thyroidectomy, extra thyroid extension of the tumour, and thyroiditis were found to be the risk factors for incidental parathyroid excision.

Keywords: incidental parathyroid excision, parathyroid hormone, parathyroid injuries


How to cite this article:
Gad SS, Elsamie MA, Saleh YA. Parathyroid gland injuries during total and subtotal thyroidectomy. Menoufia Med J 2015;28:807-12

How to cite this URL:
Gad SS, Elsamie MA, Saleh YA. Parathyroid gland injuries during total and subtotal thyroidectomy. Menoufia Med J [serial online] 2015 [cited 2020 May 31];28:807-12. Available from: http://www.mmj.eg.net/text.asp?2015/28/4/807/173595


  Introduction Top


Surgical destruction of the parathyroid glands is the most common cause of hypoparathyroidism. Hypoparathyroidism can occur after any surgical procedure that involves the anterior neck, but it is most commonly seen as a complication of parathyroid surgery or thyroid surgery or after extensive resection for head and neck cancer. Trauma to the parathyroid vascular pedicles or inadvertent removal of the glands leads to either transient or permanent hyperparathyroidism [1] .

Routine oral calcium and vitamin D were given to the patients at pant hospitalization or readmission. Supplements have been proposed to prevent the development of symptomatic hypocalcaemia and to increase the likelihood of early hospital discharge after bilateral surgical treatment of the thyroid gland [2] .

Transient symptomatic hypocalcaemia after total thyroidectomy is reported to occur in ~7-25% of the cases, whereas permanent hypocalcaemia is less common, occurring in 0.4-13.8% of the patients. There is, however, no consensus on the appropriate identification or treatment of patients with post-thyroidectomy hypocalcaemia. Infact, many patients who experience a decrease in the serum calcium are asymptomatic, and the decrease in calcium necessary to produce symptoms is variable. For example, numerous patients undergo a decrease from a preoperative normal calcium level to levels such as 8.5-9.0 mg/dl. In the absence of symptoms, this decrease is less meaningful [3] .

Estimates for transient hypoparathyroidism after thyroid surgery range from 6.9 to 46% and for permanent hypoparathyroidism from 0.4 to 33% [4] .

The remainder of the gland is minced, using a fresh #15 blade scalpel, to increase its surface area. The minced gland is then autotransplanted into a pocket of the sternocleidomastoid muscle. The pocket is closed with a nonabsorbable suture. It is important to avoid hematoma formation when forming the pocket in the sternocleidomastoid muscle because this may jeopardize the viability of the autotransplanted parathyroid gland [5] .

If morbidity during and after thyroid surgery is to be minimized or avoided, and if high rates of success are to be achieved, surgeons must have detailed knowledge of the anatomy and the embryology of the thyroid gland. The surgeon must be fully prepared to apply that knowledge during the course of operations on this organ [6] .

Branches of the inferior thyroid artery supply the parathyroids. A considerable amount of variation exists: supply by the superior thyroid arteries, the thyroid ima artery, the laryngeal arteries and `tracheal arteries or oesophageal arteries has been documented. The glands drain into the plexus of veins on the anterior surface (front) of the thyroid comprising the superior, the middle and the inferior thyroid veins [7] .

Venous drainage accompanies the venous drainage of the thyroid including capsular vessels and the larger main thyroid veins [8] .

Patients with hypoparathyroidism often display signs and symptoms of hypocalcaemia and exhibit diminished serum calcium, elevated serum phosphorus and reduced serum parathormone levels. The clinical symptoms are quite distressing, especially in severe hypoparathyroidism in which the symptoms may be life threatening [9] .

Normally, they are symmetrically arranged with the two superior parathyroids lying about 1 cm above the point where the inferior thyroid artery enters the thyroid. The two inferior parathyroid lie 1 cm below this point [10] .


  Objective Top


The aim of this study was to identify the incidence and the clinical relevance of incidental parathyroid excision during total and subtotal thyroidectomy in benign thyroid diseases such as simple multinodular goiter, secondary toxic goiter, diffuse toxic goiter relapsing after full medical treatment, selected cases of thyroiditis (Hashimoto's thyroiditis) and thyroid cancer.


  Patients and methods Top


We conducted a prospective study by collecting data from 30 patients who were admitted to the General Surgery Department, Menoufia University Hospital, during the period from 4 November 2012 to 31 March 2014.

Inclusion criteria

All the patients presented with thyroid diseases including simple multinodular goiter, diffuse toxic goiter relapsing after full medical treatment, selected cases of thyroiditis (Hashimoto's thyroiditis) and thyroid cancer.

All patients were subjected to the following:

Preoperative assessment

History taking

History taking included the age, the sex, the marital status and special habits. Symptoms evaluated included neck swelling, pressure symptoms and toxic manifestations.

Clinical examination

Both general and local function tests were performed systematically.

Laboratory investigations

Laboratory tests included thyroid function tests (T3, T4, thyroid-stimulating hormone) and serum calcium before and after the surgery.

Imaging techniques

Imaging techniques performed included ultrasound ± computed tomography ± thyroid scans.

Indirect laryngoscopy was performed before and after the surgery.

All surgical specimens were subjected to histopathology routinely. Postoperative serum calcium levels were estimated routinely after 48 h of surgery and then subsequently as required. An assessment of symptom relief, recurrent laryngeal nerve (RLN) injury, transient hypocalcaemia and permanent hyperparathyroidism was noted. Postoperative hypocalcaemia was defined as serum calcium levels less than 8.2 mg/dl (normal range 8.2-10.1 mg/dl) in our laboratory. Hormonal replacement therapy was started postoperatively. A standard dose of 100 μg was administered to both the groups, and thyroid function tests were monitored in an interval of 3 months. On the basis of the reports, titration of the dosage of l-thyroxin was carried out.

Serum calcium levels were measured preoperatively, on the day of the surgery, on postoperative days 1 and 2 and 4 to 6 weeks postoperatively in the surgical outpatient clinic. Hypocalcaemic patients were followed up for at least 6 months in the outpatient clinic to determine whether the hypocalcaemia was transient or permanent. Results were recorded and tabulated.

Postoperative hypoparathyroidism was assumed when calcium and/or vitamin D was required to treat the clinical symptoms of hypocalcaemia and it was considered permanent when calcium or vitamin D supplementation exceeded 6 months postoperatively to treat the clinical symptoms of hypocalcaemia.


  Total thyroidectomy techniques Top


Positioning of the patient

Under general anaesthesia, the patient was placed in the supine position on the operating table, placing a sand bag between the shoulders and a ring under the head so that the patient's neck is extended.

The skin is prepared with antiseptic solution (povidone iodine).

Skin incision and creation of skin flaps

The skin incision is performed two finger breadths above the clavicle and the suprasternal notch parallel to the skin crease. The incision extends between the posterior border of the sternocleidomastoid muscles. The subcutaneous tissue is cut in the same line as the skin incision and the platysma is cut slightly above the line of skin incision.

The superior skin flap is raised by applying two allis forceps on the platysma and pulling them vertically by the assistant to demonstrate the space between the platysma and the strap muscles by dissecting the superficial to the deep cervical fascia and the anterior jugular vein using the counter traction to facilitate the dissection (just above the junction between the upper flap and the underlying deep cervical fascia). Usually, we do not divide the anterior jugular vein unless it is enlarged and is interfering with dissection or the gland is huge. We use both blunt and sharp dissection with diathermy for ligating any blood vessels in the way. This is continued till the thyroid cartilage is recognized by its palpable notch.

The strap muscles are retracted laterally and upwards by two Langenbeck retractors and the lobe is pulled medially, and the space between them is developed using a pledget till the middle thyroid vein is identified (if present), which is then ligated by 3/0 synthetic absorbable ligature (Vicryl) and divided; this allows the lobe to be mobilized more medially and anteriorly.

Handling of the parathyroid glands

The superior parathyroid gland, 'untouched' with its intact supply, is dissected from the trachea; after that, the inferior thyroid within the thyroid capsule is ligated to avoid postoperative hypoparathyroidism; the parathyroid glands are preserved in situ. This is accomplished by dissecting the parathyroid glands downward away from the thyroid capsule. The vascular branches to the thyroid gland are ligated and divided close to the capsule to preserve the blood supply to the parathyroid glands.

Truncal ligation of the inferior thyroid artery should be avoided to preserve the small arterial branches to the parathyroid glands. If necessary, a small remnant of the normal thyroid tissue can be left in place to help preserve a parathyroid gland in situ.

Closure is performed by approximation of the strap muscles using interrupted or continuous Vicryl 3/0 after insertion of a rubber or tube drain in the space of the thyroid gland. The platysma is then approximated by interrupted inverted simple sutures using Vicryl 3/0 and the skin is closed by 3/0 polypropylene subcuticular sutures.

The neurovascular intersection (where the inferior thyroid artery crosses the recurrent laryngeal nerve) is identified, and a loop is placed around the trunk of the inferior thyroid artery. Slight tension applied to this loop facilitates further gentle dissection around the recurrent laryngeal nerve. This loop should be removed when the dissection has been completed. The inferior thyroid artery should be ligated not truncally, but peripherally on the capsule of the thyroid gland to preserve the vascular supply to the parathyroid glands.

In some patients, it is impossible to dissect the parathyroid gland free from the thyroid capsule with an adequate vascular supply. Such glands should be removed, cut into small pieces with a microsurgical knife, confirmed histologically, implanted into an adjacent muscle and marked by a nonabsorbable suture. In the case of an aggressive tumor with the potential for recurrence, the parathyroid gland should be autotransplanted.

The surgical outcome

All surgical specimens were subjected to histopathology routinely. During total and subtotal thyroidectomy, the parathyroid glands were identified.

Postoperative serum calcium levels were estimated routinely after 48 h of surgery and then subsequently as required. An assessment of symptom relief, RLN injury, transient hypocalcaemia and permanent hypoparathyroidism was made. Postoperative hypocalcaemia was defined as a serum calcium level less than 8.2 mg/dl (normal range 8.2-10.1 mg/dl) in our laboratory.

Bleeding during surgery was variable in both the groups as some of the glands were very vascular. Meticulous dissection was used to minimize the blood loss.

Four patients (13.4%) suffered from complications: two patients (6.7%) suffered from transient hypoparathyroidism, one patient (3.3%) from unilateral partial recurrent laryngeal nerve injury and one patient (3.3%) from difficult intubation.

Hypocalcaemia is a common occurrence after thyroidectomy. The incidence of temporary hypocalcaemia was reported to be between 6.9 and 25% [11] .

The symptoms and signs of hypoparathyroidism are mainly due to hypocalcaemia; however, cataract has been reported in as many as 70-80% of the patients with permanent hypoparathyroidism despite laboratory evidence of normocalcaemia [12] .

All our specimens showed adequate free margins, and all our cases showed no local recurrences, but this might also be due to the relatively short time of follow-up.

Cosmetic outcomes

The cosmetic appearance was scored according to both the surgeon's and the patient's satisfaction; 24 cases were scored as excellent (80%), three as good (10%) , two as fair (6.7%) and one case as having bad cosmetic results (3.3%).


  Results Top


This study included 30 patients with thyroid disease. They presented at the General Surgery Department of Menoufia University Hospital during the period from 4 December 2012 to 31 March 2014. During total thyroidectomy, the parathyroid glands were identified.

Many surgeons prefer subtotal thyroidectomy owing to the fact that the chances of permanent hypoparathyroidism are less. No permanent hypoparathyroidism was recorded; however, transient hypoparathyroidism was noted in two patients with total thyroidectomy, which was managed with calcium gluconate infusion ([Table 1]).
Table 1 Characteristics of the studied sample


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We found two cases with temporary hypocalcaemia with Hashimoto thyroiditis and medullary carcinoma ([Table 2]). The typical signs and symptoms associated with hypocalcaemia are neuromuscular irritability, including perioral or acral paresthesia, muscle cramps that may progress to carpopedal spasm, laryngospasm, bronchospasm or even tetany ([Table 3]).
Table 2 Preoperative calcium levels in the studied sample


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Table 3 The postoperative calcium status in the studied sample


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After giving intravenous calcium salts using one ampoule of calcium gluconate in 1 l of 5% dextrose at an initial infusion rate of 100 ml/h, we observed a good response and improvement in cases on monitoring the calcium level.


  Discussion Top


In the present study, risk factors for incidental parathyroid excision included total thyroidectomy, Hashimoto thyroiditis and extrathyroid spread. As expected in total thyroidectomy, bilateral dissection increased the risk of parathyroid removal. This may be related to the fact that dissection bilaterally puts all four glands at risk.

In addition, in the current study, total thyroidectomy was performed mainly for malignant thyroid disease, and malignancy was reported to be a strong predictor of incidental parathyroid excision in earlier studies, although it was not a risk factor in our study.

The minimally invasive or focused approach to parathyroid surgery requires a thorough understanding of the anatomic relationships of the parathyroid glands to adjacent landmark structures, including the recurrent laryngeal nerve and the inferior thyroid artery [13] .

Routine identification of fewer than three parathyroid glands resulted in increased rates of permanent hypocalcaemia [14] .

Identification of at least one parathyroid gland was not associated with significantly lower rates of transient or permanent hypoparathyroidism [15] .

As postoperative hypoparathyroidism is a well-recognized complication in thyroid surgery, preservation of the parathyroid blood supply has been among the aims of successful thyroid surgery; this issue has existed since a long time, and led the eminent surgeon Halsted in year 1907 to ask the question as to whether 'Thyroid vessels must be ligated somewhere. Should they be so ligated as not to cut off the blood supply of parathyroid glandules? Replying to this question is impossible without definite knowledge of the blood supply to these little bodies' [16] .

To preserve the integrity of the blood supply to parathyroid glands, much argument has been found regarding the level of division of the inferior thyroid artery during bilateral thyroid surgery on parathyroid function. Many authors, however, prefer to ligate the inferior thyroid artery peripherally, that is, close to the thyroid capsule. They claim that unlike central ligation near the offspring from the external carotid artery, peripheral ligation of the inferior thyroid artery preserves the integrity of the parathyroid blood supply better [17] .

Many researchers have tried to determine the incidence of post-thyroidectomy hypoparathyroidism (both transient and permanent) and factors that influence this incidence. Owing to the fact that 80% of the parathyroid blood supply of the four parathyroid glands is derived from the inferior thyroid artery, the effect of the level of ligation and the division of the inferior thyroid artery during bilateral thyroid surgery on the parathyroid function has attracted much attention of researchers.

Many researchers have reported that the incidental parathyroid excision group had significantly lower postoperative calcium levels, and this is in line with our findings. Injury, devascularization and incidental parathyroid gland excision of the parathyroids have all been reported as causes of postoperative hypocalcaemia. Although other specific factors have been studied, the cause of postoperative hypocalcaemia remains multifactorial. The overall incidence of permanent hypocalcaemia among our patients was 2.1%. Although hypocalcaemia reverses spontaneously in most patients, it can remain permanent when caused by an irreversible injury to the parathyroid glands.

The morphologic features and the function of the thyroid gland, central neck dissection, experience of the surgeon and parathyroid autotransplantation do not influence the development of postoperative hypoparathyroidism. In our series, no permanent hypoparathyroidism was recorded; however, transient hypoparathyroidism was noted in two patients in total thyroidectomy, which is in the normal range as per the literature ([Figure 1], [Figure 2], [Figure 3]).
Figure 1 Blood supply of parathyroid glands.



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Figure 2 Actions of the major calcium-regulating hormone.



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Figure 3 Surgical anatomy of the parathyroid glands.



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  Conclusion Top


The minimally invasive or focused approach to parathyroid surgery requires a thorough understanding of the anatomic relationships of the parathyroid glands to adjacent landmark structures, including the recurrent laryngeal nerve and the inferior thyroid artery [18] .

Incidental parathyroid excision during thyroid resection is not uncommon, and it occurred in 16.4% of the cases in this series. Total thyroidectomy, extrathyroid extension of the tumor and thyroiditis were found to be risk factors for incidental parathyroid excision.

Total thyroidectomy is recommended as a routine procedure of choice in benign thyroid diseases because it avoids leaving residual unhealthy thyroid tissue liable for recurrence with or without superimposed malignancy and no injury to the parathyroid gland [19] .


  Acknowledgements Top


Conflicts of interest

None declared.

 
  References Top

1.
Clark OH, Duh QY, Kebebew E. Occurrence and prevention of complications in thyroidectomy (2005), p207.  Back to cited text no. 1
    
2.
Roh JL, Park CI. Routine oral calcium and vitamin D supplements for prevention of hypocalcemia after total thyroidectomy. Am J Surg 2006; 192 :675-678.  Back to cited text no. 2
    
3.
Pelizzo MR, Piotto A, Toniato A. PTH assay in the first postoperative day after thyroidectomy early predictor postoperative hypocalcemia? Ann Ital Chir 2003; 74 :511-515.  Back to cited text no. 3
    
4.
Rosato, L. Complications of total thyroidectomy: incidence, prevention and treatment. Chir Ital 2002; 54 :635-642.  Back to cited text no. 4
    
5.
Carling T, Donovan P, Rinder C, Udelsman R. Minimally invasive parathyroidectomy using cervical block: reasons for conversion to general anesthesia. Arch Surg 2006; 141 :401-404 discussion 404.  Back to cited text no. 5
    
6.
Mansberger AR Jr, Wei JP. Surgical anatomy and embryology of the thyroid and parathyroid gland. In: JE Skandalakis. Surg Clin North Am 1993; 73 :727-46.  Back to cited text no. 6
    
7.
Sippel RS, Bianco J, Chen H. Radioguided parathyroidectomy for recurrent hyperparathyroidism caused by forearm graft hyperplasia. J Bone Miner Res 2003; 18 :939-942.  Back to cited text no. 7
    
8.
Terris DJ, Gourin CG, Chin E. Minimally invasive thyroidectomy: basic and advanced techniques. Laryngoscope 2006; 116 :350-356.  Back to cited text no. 8
    
9.
MJ M, Clark OH, Duh QY. Text book of endocrine surgery. 2nd ed. Philadelphia: Elsevier Saunders; 2005. p424.  Back to cited text no. 9
    
10.
Geeta Lal, Orlo H. Clark Thyroiditis. Chapter 5 ,Textbook of Endocrine, Surgery editor Orlo H. Clark, Quan-Yang Duh 2nd ed, Elsevier Saunders Philadelphia 2005344 4.  Back to cited text no. 10
    
11.
Jacobs JK, Aland JW Jr, Ballinger JF. Total thyroidectomy. A review of 213 patients. Ann Surg 1983; 197 :542-549.  Back to cited text no. 11
    
12.
Schwartz AE, Friedman EW. Preservation of the parathyroid glands in total thyroidectomy. Surg Gynecol Obstet. 1987; 165 :327-332.  Back to cited text no. 12
    
13.
Lennquist S. Total thyroidectomy with safe preservation of the laryngeal nerves and parathyroid glands. Chicago: American College of Surgeons film Library; 1991.  Back to cited text no. 13
    
14.
Thomusch O, Machens A, Sekulla C. Multivariate analysis of prognostic factors in benign goiter surgery for postoperative complications. World J Surg 2000; 24 :1335-1341.  Back to cited text no. 14
    
15.
Trupka A, Sienel W. Autotransplantation of at least one parathyroid gland during thyroidectomy in benign thyroid disease minimizes the risk of permanent hypoparathyroidism. Zentralbl Chir 2002; 127 :439-442.  Back to cited text no. 15
    
16.
Sciumè C, Geraci G, Pisello F, Facella T, Li Volsi F, Licata A, Modica G. Complications in thyroid surgery: symptomatic post-operative hypoparathyroidism incidence, surgical technique, and treatment. Ann Ital Chir 2006; 77 :115-122.  Back to cited text no. 16
    
17.
Casella C, Talarico C, Di Fabio F, Bugari G, Iacobello C, Albertini A, Salerni B. Hypoparathyroidism following total thyroidectomy: prognostic value of intraoperative parathyroid hormone assay. Ann Ital Chir 2004; 75 :23-27.  Back to cited text no. 17
    
18.
Ogilvie JB, Clark OH. Parathyroid surgery: we still need traditional and selective approaches. J Endocrinol Invest 2005; 28 :566-569.  Back to cited text no. 18
    
19.
Sultan HM, El-Kader Ahmed HA, Sedhom HI. Evaluation of total thyroidectomy in benign thyroid diseases. Menoufia Med J 2014; 27 :205-207.  Back to cited text no. 19
    


    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

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Abstract
Introduction
Objective
Patients and methods
Total thyroidect...
Results
Discussion
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