ORIGINAL ARTICLE Near-Total Thyroidectomy Could Be the Best Treatment for Disease in Endemic Regions

Zeki Acun, MD; Mustafa Comert, MD; Alper Cihan, MD; Suat Can Ulukent, MD; Bulent Ucan, MD; Guldeniz Karadeniz C¸ akmak, MD

Hypothesis: Near-total thyroidectomy, on the basis of Results: In our clinic, near-total thyroidectomy was the its low morbidity rate, is an appropriate treatment op- principal surgical procedure performed for benign thy- tion in the surgical management of various thyroid dis- roid disease. The temporary recurrent laryngeal nerve eases in an endemic region in Turkey. palsy rate with respect to the nerves at risk was 3.3% (10 of 304 nerves), whereas temporary Design: Single-institution study of patients with vari- was 7.2% (11 of 152 patients). Neither permanent re- ous thyroid diseases treated by means of near-total thy- current laryngeal nerve palsy nor permanent hypopar- roidectomy within 2 years in an endemic region, with athyroidism occurred. In 1 patient, wound hematoma de- comparison of the results vs the complication rates of bi- veloped and required re-exploration. Seroma in another lateral subtotal and total thyroidectomy reported in the patient needed no medical or surgical intervention. Nei- literature. ther wound nor mortality were noted.

Setting: Tertiary academic referral center. Conclusions: Near-total thyroidectomy achieves a lower complication rate of hypoparathyroidism and a similar Patients: One hundred fifty-two patients who under- complication rate of recurrent laryngeal nerve palsy and went near-total thyroidectomy for various thyroid dis- recurrence when compared with the rates reported in the eases. literature for total thyroidectomy. It is an effective and safe surgical treatment option for various benign thy- Main Outcome Measures: Surgical treatments of vari- roid diseases. ous benign thyroid diseases were compared according to the complication rates and the achievable benefits of the procedures. Arch Surg. 2004;139:444-447

EALTH PROBLEMS RELATED An important disadvantage of total to the thyroid are thyroidectomy is the high incidence of hy- common. Goiter preva- pocalcemia due to lence is reported to range devascularization.7 A low complication rate from 5% to 56% in Tur- is the advantage of subtotal thyroidec- key.H1 Many treatment modalities have been tomy, but secondary thyroidectomy may described for the surgical management of be necessary because of recurrence after various thyroid diseases, including exci- subtotal thyroidectomy and is associated sion, bilateral subtotal thyroidectomy, near- with increased morbidity and related to total thyroidectomy, and total thyroidec- tomy. However, the use of should See Invited Critique always be based on the achievable benefits at end of article of the procedure and outweigh the poten- tial complications. All of the treatment al- recurrent laryngeal nerve injury and hy- ternatives achieve different kinds and inci- poparathyroidism resulting from par- dences of morbidities. As a result, most athyroid gland devascularization.8 The surgeons have been looking for a treat- goal of this study is to evaluate near-total From the General Surgery ment that results in the least recurrence and thyroidectomy as an appropriate treat- Department, School of lowest complication rate. Total thyroidec- ment for thyroid disorders in endemic Medicine, Zonguldak tomy for management of benign thyroid dis- regions in Turkey because its recurrence Karaelmas University, orders is increasingly accepted, although the rate is lower than that of subtotal thy- Zonguldak, Turkey. indications are not well defined.2-6 roidectomy and there is a lower possibil-

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©2004 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/27/2021 Table 1. Indications for Surgical Treatment Table 2. Clinical Signs in 152 Patients

Indication No. (%) of Patients Clinical Sign No. (%) of Patients Suspicious or indefinite cytologic findings 0 Thyroid function test results Compressive symptoms 58 (38.2) Euthyroidism 86 (56.6) Recent enlargement 14 (9.2) 66 (43.4) Cosmesis 14 (9.2) 0 Toxic multinodular goiter 66 (43.4) Ultrasonographic evaluation results Total 152 (100) Multinodular goiter 96 (63.2) Solitary nodules 53 (34.9) Diffuse goiter 3 (2.0)

ity of parathyroid damage when it is compared with that of total thyroidectomy. Table 3. Postoperative Complications METHODS Complication No. (%) of Patients Between April 15, 2001, and May 15, 2003, 152 patients with goiter who underwent surgical treatment in our clinic (Gen- Recurrent laryngeal nerve palsy eral Surgery Department, Zonguldak Karaelmas University, Temporary 10 (6.6)* School of Medicine, Zonguldak, Turkey) were included in this Permanent 0 study. All patients provided informed consent. All patients were Hypoparathyroidism evaluated by means of physical examination, thyroid function Temporary 11 (7.2) tests, thyroid ultrasonography, and thyroid scintigraphy. Fine- Permanent 0 Wound hematoma 1 (0.7) needle aspiration was performed for hypoactive and domi- Bleeding 0 nant thyroid nodules. In our surgical department, we per- Wound infection 0 formed total thyroidectomy in single nodules that were suspected Seroma 1 (0.7) of malignancy at fine-needle aspiration biopsy; therefore, these Total 23 (15.2) patients were specifically excluded. Antithyroid medications were used for hyperthyroidism before surgery to attain euthy- *The rate of temporary recurrent laryngeal nerve palsy was 3.3% with roidism. respect to the nerves at risk. Videolaryngostroboscopic examinations were performed to evaluate vocal cord motility 24 hours before surgery and 48 hours after surgery in all patients and included confirmation topathologically. Intraoperative frozen section evalua- of normal vocal cord movement in patients who had tempo- tions were used for nodules suspected of being malig- rary neuropraxia. Near-total thyroidectomy was performed in nant that had not been suspected of being malignant all cases and consisted of total lobectomy in the lobe having the dominant nodule, with isthmectomy and near-total lobec- preoperatively; there was no malignancy at frozen sec- tomy in the contralateral side, leaving a small quantity of about tion evaluation. Parathyroid autotransplantation was per- 2 g of thyroid tissue adjacent to the parathyroid and their formed in 7 patients, and none developed temporary or blood supply. Recurrent laryngeal nerves in all cases were iden- permenant hypoparathyroidism. tified and traced to the cricoid cartilage in either side. Every Postoperative complications are summarized in attempt was made to demonstrate and preserve all of the par- Table 3. The temporary recurrent laryngeal nerve palsy athyroid glands with their blood supply. When a parathyroid rate with respect to the nerves at risk was 3.3% (10 of gland was damaged, it was transplanted into the sternocleido- 304 nerves), whereas temporary hypoparathyroidism was mastoid muscle. 7.2% (11 of 152 patients). Neither permanent recurrent In each patient, serum calcium and phosphorus levels were laryngeal nerve palsy nor permanent hypoparathyroid- checked on the first and second postoperative days. Hypocal- cemia is defined as low ionized serum calcium levels and the ism occurred. Wound hematoma developed in 1 patient presence of symptoms of hypocalcemia. We considered hypoc- and required re-exploration. Seroma in another patient alcemia temporary when it lasted about 3 to 6 weeks after sur- needed no medical or surgical intervention. Five papil- gery. Calcium levels were followed up in patients who were tem- lary carcinomas in 4 female patients and 1 male patient porarily hypocalcemic and who needed calcium supplements. were diagnosed by using paraffin blocks. We performed iodine I 131 ablation in these patients. Neither wound RESULTS infection nor mortality was noted.

There were 113 female and 39 male patients, with a mean COMMENT age of 43 years (range, 24-77 years). We performed near- total thyroidectomy in all patients; the various indica- The surgical treatment of benign is still tions are summarized in Table 1. The clinical signs in controversial. Many treatments have been described for these patients are summarized in Table 2. Sixty-six pa- the surgical management of multinodular goiter, includ- tients were treated medically because of hyperthyroid- ing unilateral or bilateral subtotal thyroidectomy, hemithy- ism to achieve euthyroidism preoperatively. Thyroid scin- roidectomy, near-total thyroidectomy, and total thy- tigraphy depicted hypoactive nodules in 73 patients. Fine- roidectomy. Despite numerous studies of operative needle aspiration biopsy was performed in 87 patients, strategies, we still do not have clear evidence about which and the results were neither suspected nor malignant his- option is the best. When the disorder affects both lobes,

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©2004 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/27/2021 total or near-total thyroidectomy is mandatory, espe- ablation. An advantage of near-total thyroidectomy over sub- cially in younger persons, to obviate suppressive therapy total thyroidectomy is that the thyroid remnant of about and possible relapse. Subtotal thyroidectomy may be 2 g renders it accessible to 131I ablation if is found the best elective procedure in older patients to avoid to- in the specimen and obviates reoperation for completion tal and permanent dependence on drugs.9 Some authors thyroidectomy.25 favor the subtotal procedure in the treatment of benign Permanent or temporary hypoparathyroidism is a multinodular disease because of its lower incidence of well-known complication of total thyroidectomy. Exci- iatrogenic injuries such as recurrent nerve palsy and sion of parathyroid glands and vascular insufficiency are hypoparathyroidism and the supposed autonomous eu- the main causes of this complication. Although we would thyroidism requiring no medical intervention.7 Other have liked to compare complication ratios between to- authors advocate total thyroidectomy because the inci- tal thyroidectomy and near-total thyroidectomy in our dence of iatrogenic injuries is similar to that of the sub- surgical department, it was not appropriate because we total procedure, and there is no risk of recurrence.10-12 had an insufficient number of patients who underwent Recurrence that requires further resection is a rel- total thyroidectomy. To compare our complication ra- evant factor in the choice of operation. It is difficult to tios, especially temporary hypoparathyroidism after near- evaluate the results of thyroid surgery for benign dis- total thyroidectomy with that after total thyroidectomy, ease mainly because of the long follow-up required for we used reports of total thyroidectomy of both current complete assessment of the outcome when there may be and past authors. a delay of 20 or 30 years before recurrence.13 According According to our review of the literature, tempo- to our review of the literature, recurrence develops in as rary hypocalcemia ranged from 24% to 35% after total many as 14.5% of cases after subtotal resection, despite thyroidectomy.2-6,22,26,27 Even the lowest rate of tempo- drug prophylaxis; without suppressive therapy, the rate rary hypocalcemia after total thyroidectomy in the lit- of recurrence increases to 43%.6,14 Ambrosi et al15 found erature is nearly 3 times higher than the rate of tempo- that recurrence was inversely related to the extent of re- rary hypocalcemia in our series. The incidence of section. Piraneo et al14 reported a 39% recurrence rate permanent hypoparathyroidism ranged from 0% to 0.2% after enucleation, 27% after lobectomy, 20% after lobec- after subtotal resection and from 0% to 3.8% after total tomy and contralateral enucleating excision, and 4% af- resection.7 The incidence of permanent recurrent laryn- ter subtotal resection. Recurrence rates after subtotal thy- geal nerve injuries after subtotal and total procedures var- roidectomy vary as much as 14%.16 Recurrence after ied from 0% to 1% and from 0% to 1.3%, respec- subtotal thyroidectomy compels patients to undergo sec- tively.7,24 Neither permanent recurrent laryngeal nerve ondary thyroidectomy. palsy nor permanent hypoparathyroidism occurred in our When compared with primary thyroid surgery, sec- series. ondary thyroidectomy has an increased risk of compli- We performed near-total thyroidectomy in all of our cations, such as recurrent laryngeal nerve injury and hy- patients. The central premise of our study is the balance poparathyroidism.8 The best means of diminishing the of leaving a small quantity of thyroid tissue adjacent to complication rate is prevention through excising all patho- the parathyroid glands and their blood supply to mini- logically altered tissue.17-19 Simple excision of a nodule mize the risk of complications—principally, permanent or subtotal unilateral lobectomy should no longer be rec- and temporary hypoparathyroidism. Identification of the ommended in primary thyroid surgery. For diffuse mul- parathyroid glands and meticulous surgical technique to tinodular goiter, the thyroidectomy must be sizable be- preserve parathyroid circulation are essential during near- cause the rate of recurrence is greater than 10% after 10 total thyroidectomy. years and is directly related to the size of the thyroid rem- The lower rate of temporary hypoparathyroidism in nant.14,20 The risk of damaging the recurrent laryngeal near-total thyroidectomy when compared with that in to- nerve is far higher during a second intervention because tal thyroidectomy is an advantage because the patients of the anatomic disturbance with scar tissue left behind need shorter postoperative hospitalization and medical after the first operation and degenerative changes.21 High treatment. This decreased cost is particularly important rates of temporary (15.5%-23.6%) and permanent (2.6%- in our endemic region in Turkey because we have a great 15.5%) damage of the recurrent laryngeal nerve have been number of patients and limited medical services. Near- reported in secondary thyroidectomy.22,23 total thyroidectomy adds the advantages of total thy- The indications for total thyroidectomy for manag- roidectomy (no recurrence) to those of subtotal thy- ing benign thyroid disorders are not well defined; in fact, roidectomy (low incidence of temporary and permanent they are evolving.22,24 If a patient had an indication for to- hypoparathyroidism). In conclusion, being aware of the tal thyroidectomy that was described in the literature (ie, advantages and disadvantages of both total and subtotal history of head and neck irradiation, a multinodular thy- thyroidectomy, we propose near-total thyroidectomy for roid gland that grossly involves both lobes, locally ad- the surgical management of multinodular goiter in en- vanced disease with compressive symptoms, and nodules demic regions. highly suspected of being malignant), we performed total thyroidectomy. In our surgical department, we have a fairly Accepted for publication November 4, 2003. low rate of indications for total thyroidectomy. In most pa- Corresponding author: Zeki Acun, MD, General Sur- tients, we performed near-total thyroidectomy without sus- gery Department, School of Medicine, Zonguldak Karael- pecting malignancy; however, we found papillary carci- mas University, 67600 Kozlu, Zonguldak, Turkey (e-mail: noma in paraffin blocks for 5 patients and performed 131I [email protected]).

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©2004 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/27/2021 its role in the management of thyroid disease. AustNZJSurg. 1992;62:91-95. REFERENCES 14. Piraneo S, Vitri P, Galimberti A, Guzzetti S, Salvaggio A, Bastagli A. Recurrence of after operation in euthyroid patients. Eur J Surg. 1994;160:351-356. 1. Erdogan G, Erdogan MF, Emral R, et al. Iodine status and goiter prevalence in 15. Ambrosi A, Pezzolla A, Barone G, et al. Studio clinico della funzione residua e Turkey before mandatory iodization. J Endocrinol Invest. 2002;25:224-228. delle recidive in pazienti operati di tiroidectomie parziali per struma nodulare eu- 2. Mishra A, Agarwal A, Agarwal G, Mishra SK. Total thyroidectomy for benign thy- tiroideo. Ann Ital Chir. 1994;65:543-547. roid disorders in an endemic region. World J Surg. 2001;25:307-310. 16. Bistrup C, Nielsen JD, Gregersen G, Franch P. Preventive effect of 3. Delbridge L, Guinca AI, Reeve TS. Total thyroidectomy for bilateral benign mul- in patients operated for non-toxic goitre: a randomized trial of one hundred pa- tinodular goiter. Arch Surg. 1999;134:1389-1393. tients with nine years follow-up. Clin Endocrinol (Oxf). 1994;40:323-327. 4. Mu¨ller PE, Kabus S, Robens E, Spelsberg F. Indications, risks, and acceptance 17. Wilson DB, Staren ED, Prinz RA. Thyroid reoperations: indications and risks. Am of total thyroidectomy for multinodular benign goiter. Surg Today. 2001;31:958- Surg. 1998;64:674-679. 962. 18. Teuscher J, Peter HJ, Gerber H, Berchtold R, Studer H. Pathogenesis of nodular 5. Hisham AN, Azlina AF, Aina EN, Sarojah A. Total thyroidectomy: the procedure goiter and its implications for surgical management. Surgery. 1988;103:87-93. of choice for multinodular goitre. Eur J Surg. 2001;167:403-405. 19. Kraimps JL, Marechaud R, Gineste D, et al. Analysis and prevention of recurrent 6. Pappalardo G, Guadalaxara A, Frattaroli FM, Illomei G, Falaschi P. Total com- goiter. Surg Gynecol Obstet. 1993;176:319-322. pared with subtotal thyroidectomy in benign nodular disease: personal series 20. Ro¨jdmark J, Jarhult J. High long-term recurrence rate after subtotal thyroidec- and review of published reports. Eur J Surg. 1998;164:501-506. tomy for nodular goitre. Eur J Surg. 1995;161:725-727. 7. Foster RS Jr. Morbidity and mortality after thyroidectomy. Surg Gynecol Obstet. 21. Katz AD, Bronson D. Total thyroidectomy: the indications and results of 630 cases. 1978;146:423-429. Am J Surg. 1978;136:450-454. 8. Beahrs OH, Vandertoll DJ. Complications of secondary thyroidectomy. Surg Gy- 22. Liu Q, Djuricin G, Prinz RA. Total thyroidectomy for benign thyroid disease. Sur- necol Obstet. 1963;117:535-539. gery. 1998;123:2-7. 9. Pelizzo MR, Bernante P, Toniato A, Fassina A. Frequency of thyroid carcinoma 23. Reeve TS, Delbridge L, Brady P, Crummer P, Smyth M. Secondary thyroidec- in a recent series of 539 consecutive thyroidectomies for multinodular goiter. tomy: a twenty-year experience. World J Surg. 1988;12:449-453. Tumori. 1997;83:653-655. 24. Perzik S. The place of total thyroidectomy in the management of 909 patients 10. Jacobs J, Aland J, Ballinger J. Total thyroidectomy: a review of 213 patients. Ann with thyroid disease. Am J Surg. 1976;132:480-483. Surg. 1983;197:542-549. 25. Menegaux F, Turpin G, Dahman M, et al. Secondary thyroidectomy in patients 11. Karlan M, Katz B, Dunkelman D, Uyeda R, Gleischman S. A safe technique for with prior thyroid surgery for benign disease: a study of 203 cases. Surgery. 1999; thyroidectomy with complete nerve dissection and parathyroid preservation. Head 126:479-483. Neck Surg. 1984;6:1014-1021. 26. Reeve TS, Delbridge L, Cohen A, Crummer P. Total thyroidectomy: the preferred 12. Perzik SL, Katz B. The place of total thyroidectomy in the management of thy- option for multinodular goiter. Ann Surg. 1987;206:782-786. roid disease. Surgery. 1967;62:436-440. 27. La Gamma A, Letoquart JP, Kunin N, Chaperon J, Mambrini A. Nodular goiter: retro- 13. Khadra M, Delbridge L, Reeve TS, Poole AG, Crummer P. Total thyroidectomy: spective analysis of 608 cases [in French]. J Chir (Paris). 1993;130:391-396.

Invited Critique

otal thyroidectomy for bilateral nodular goiter has become the preferred surgical approach in many centers.1 This is T because as many as 20% of incompletely resected bilateral goiters after lobectomy or subtotal thyroidectomy recur, thyroid therapy for thyroid-stimulating hormone suppression does not appear to reduce the risk of postoperative recurrence, and thyroid reoperation for recurrent goiter may be associated with a higher risk of complications.2-4 Although total thyroidectomy offers these advantages, the risk of complications from total thyroidectomy is considered by some to be higher than that from less extensive resections. Acun and colleagues report their results for near-total thyroidectomy in patients with benign nodular thyroid disease and conclude that, compared with total thyroidectomy, near-total thyroidectomy achieves a lower rate of hypoparathyroid- ism (7.2% transient) and similar rates of recurrent laryngeal nerve injury (6.6% transient) and recurrence. The investigators should be applauded for comprehensive and objective documentation of complications associated with near-total thyroidec- tomy. Unfortunately, the comparison of near-total thyroidectomy complications in the authors’ experience to that published for total thyroidectomy provides no evidence-based conclusions or recommendations. At the least, the authors should pro- vide a systematic review or meta-analysis of the literature. The investigators show that near-total thyroidectomy for benign nodular thyroid disorders is a relatively safe operation at their institution without any long-term morbidity, but the difference in risk of complications, as compared with that for total thyroidectomy, remains to be determined. Although the authors conclude that near-total thyroidectomy has a similar recurrence rate as does total thyroidectomy, albeit a low risk given the small thyroid remnant of 2 g, their study does not provide the long-term follow-up data to make such a conclusion. Given existing evidence for the surgical outcome of treat- ing benign nodular thyroid disorders, the extent of thyroidectomy should be tailored to the indications for the procedure, patient preference based on a discussion of the risks and benefits of the different extents of thyroidectomy, and the surgeon’s experience in performing these procedures.

Electron Kebebew, MD San Francisco, Calif

1. Reeve TS, Delbridge L, Cohen A, Crummer P. Total thyroidectomy: the preferred option for multinodular goiter. Ann Surg. 1987;206:782-785. 2. Marchesi M, Biffoni M, Faloci C, Biancari F, Campana FP. High rate of recurrence after lobectomy for solitary . Eur J Surg. 2002;168:397-400. 3. Hegedus L, Bonnema SJ, Bennedbaek FN. Management of simple nodular goiter: current status and future perspectives. Endocr Rev. 2003;24:102-132. 4. Wilson DB, Staren ED, Prinz RA. Thyroid reoperations: indications and risks. Am Surg. 1998;64:674-679.

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