International Journal of Pediatric Otorhinolaryngology 78 (2014) 1742–1746

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Nodular recurrence and hypothyroidism following partial thyroidectomy for benign nodular thyroid disease in children and adolescents M. Akkari a,*, D. Schmitt a, C. Jeandel b, I. Raingeard c, C. Blanchet a, C. Cartier a, R. Garrel a, B. Guerrier a, M. Makeieff a, M. Mondain a a Service d’ORL et Chirurgie Cervico Faciale, CHU de Montpellier, Universite´ Montpellier 1, Hoˆpital Gui de Chauliac, 80 avenue Augustin Fliche, 34295 Montpellier Cedex 5, France b Service d’Endocrinologie Pe´diatrique, CHU de Montpellier, Universite´ Montpellier 1, Hoˆpital Arnaud de Villeneuve, 371 avenue du Doyen Gaston Giraud, 34295 Montpellier Cedex 5, France c Service des maladies endocriniennes, CHU de Montpellier, Universite´ Montpellier 1, Hoˆpital Lapeyronie, 371 avenue du Doyen Gaston Giraud, 34295 Montpellier Cedex 5, France

A R T I C L E I N F O

A B S T R A C T

Article history: Received 18 June 2014 Received in revised form 17 July 2014 Accepted 31 July 2014 Available online 8 August 2014

Objectives: Diagnostic and therapeutic processing of a thyroid nodule in children and adolescents may require lobectomy–isthmusectomy (LI) or nodule-resection (NR). Very few data in the literature report the long-term evolution of the remaining thyroid lobe in a defined pediatric population. In this study, we aimed to answer the following questions: Does a nodule recurrence occur in the remainder lobe? Is a post-operative thyroxine treatment necessary? Material and methods: This retrospective study describes 28 patients under 18 who underwent LI (22 cases) or NR (6 cases) from January 2004 to March 2012. Ten of them were lost to follow up, 18 could be assessed (4 NR (22%) and 14 LI (78%) - mean follow-up 45  31 months). All patients benefited of postoperative thyroid ultrasonography, and regular endocrinologic follow-up. The following data were analysed: emergence of new thyroid nodules, evolution of pre-existing nodules, occurrence of post-operative hypothyroidism and requirement for completion thyroidectomy. Results: The mean age at the time of surgery was 14.3  1.9 years. Two patients (11%) had pre-existing nodules in the remaining thyroid gland, none of which showed an increase in size after surgery. De novo nodules developed in five patients (27.8%). Three patients who underwent LI (21.4%) needed thyroxine treatment for post-operative hypothyroidism. One patient (5.5%) needed completion thyroidectomy. Conclusions: In this children and adolescents population, after performing LI or NR, remaining thyroid tissue stays free of nodules in 72.2% of the cases. A post-operative thyroxin treatment is necessary in 21.4% of cases after LI. ß 2014 Elsevier Ireland Ltd. All rights reserved.

Keywords: Thyroid nodule Children Lobectomy–isthmusectomy Nodule resection Hypothyroidism Post-operative thyroxin treatment

1. Introduction The prevalence of nodular disease in children is 1.5% [1]. Indications for thyroid surgery for single or multiple nodular disease in adults are: occurrence of compressive symptoms (dysphagia, dyspnea, vascular compression), thyroid disease refractory to medical treatment, aesthetic discomfort and suspicion of malignancy. The latter is at the forefront in children and

* Corresponding author. Tel.: +33 4 67 33 68 04; fax: +33 4 67 33 67 28. E-mail address: [email protected] (M. Akkari). http://dx.doi.org/10.1016/j.ijporl.2014.07.037 0165-5876/ß 2014 Elsevier Ireland Ltd. All rights reserved.

adolescents according to malignancy rates described in the literature as higher than in adults [2]. In case of unilateral disease and benign histology, several reports suggest partial thyroidectomy, in both adults and children [3,4]: lobectomy–isthmusectomy (LI) or nodule resection (NR) when a single nodule is easily accessible. The fate of the remaining thyroid tissue after partial surgery has been reported in numerous studies in adults, concerning nodular recurrences [5,6], and occurrence of postoperative hypothyroidism [7,8]. However, reports on this subject including a pediatric population were rather focused on immediate surgery complications and malignancy rate [9]; there are no data

M. Akkari et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 1742–1746

regarding long-term evolution of the remaining thyroid tissue and thyroid function. We hypothesize that this evolution might differ from an adult population. The purpose of our study is to answer the following two questions: What is the recurrence rate of nodular disease on the remaining lobe and what are the associated risk factors? What is the post-operative rate of hypothyroidism, requiring Levo-T4 (L-T4) substitutive therapy, with which risk factors?

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– TSH pre-operative value (mean interval between pre-operative TSH measurement and surgery: 4  5 months); – TSH post-operative value (mean interval between surgery and post-operative TSH measurement: 2  2 months); – Existence of a post-operative L-T4 therapy and its indication. We sought to highlight the influence of risk factors for postoperative hypothyroidism (pre-operative and post-operative TSH levels, multiple nodules, thyroiditis features on histological analysis) by comparing the groups ‘‘need for post-operative L-T4 therapy’’ and ‘‘no need for post-operative L-T4 therapy’’ All statistical tests were performed with the SAS Statview1 software for Windows. Quantitative data were compared between groups by the Mann–Whitney Wilcoxon test. The comparison between two qualitative parameters was performed using the Fisher exact test. Significance level was determined for a p value or = 18 years). Histopathological results and surgical follow up data (reinterventions) were also collected. We sought to highlight the influence of risk factors for recurrence of nodular disease (family history of thyroid nodular disease, female gender, age less than 14 years at surgery, multiples nodules, L-T4 substitutive therapy, polymorphic vesicular hyperplasia on histopathological results), by comparing the groups ‘‘occurrence of new nodules’’ and ‘‘no occurrence of new nodules’’. The following endocrinological data were collected for 14 patients who underwent LI: Table 1 Risk factors for nodular recurrence. Risk factor

‘‘Occurrence of new nodule’’ group n = 5

‘‘No occurrence of new nodule’’ group n = 13

p Value

Family history of thyroid nodular disease (n = 1) Female (n = 14) Age under 14 (n = 7) Multiple nodules (n = 7) Substitutive L-T4 treatment (n = 3) Polymorphic vesicular hyperplasia on histopathological analysis (n = 10)

0 5 4 4 1 4

1 9 3 3 2 6

1 0.28 0.04 0.04 1 0.31

(0%) (100%) (80%) (80%) (20%) (80%)

(8%) (69%) (23%) (23%) (15%) (46%)

M. Akkari et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 1742–1746

1744 Table 2 Pre and post-operative TSH values. Patients

Pre-operative TSH in IU/L

Post-operative TSH in IU/L (time elapsed since surgery in days)

For patients with post-operative hypothyroidism: TSH before starting hormone replacement therapy in IU/L (time elapsed since surgery in days)

1 2 3 4 5 6 7 8 9 10 11

1.81 2.72 1.49 1.28 1.36 3.38 0.72 1.70 0.20 1.58 1.18

1.56 3.45 3.20 1.29 4.74 4.63 1.54 3.42 3.39 1.93 1.59

X X X X X 11.02 (123) X 8.59 (297) 16.01 (85) X X

(36) (33) (28) (106) (48) (34) (246) (35) (42) (34) (34)

Table 3 Risk factors for post-operative hypothyroidism. Risk factor

‘‘Need for post-operative L-T4 treatment’’ Group n = 3

‘‘No need for post-operative L-T4 treatment’’ Group n = 11

p Value

Mean pre-operative TSH level (UI/L) Mean post-operative TSH level (UI/L) Multiple nodules (n = 5) Thyroiditis on histopathological analysis (n = 1)

1.76 3.81 3 (100%) 1 (33%)

1.46 2.41 2 (18%) 0 (0%)

0.73 0.19 0.027 0.21

3.2. Post-operative hypothyroidism Pre and post-operative TSH values were available in 11 patients out of 14. All of these patients were euthyroid before surgery (TSH value between 0.15 and 5 mIU/L). Mean pre-operative TSH value was 1.58  0.87 mIU/L (min 0.20, max 3.38). Mean post-operative TSH value was 2.79  1.27 mIU/L (min 1.29, max 4.63). Among the 14 patients followed-up, 3 (21.4%) received a postoperative L-T4 treatment. It was required for treating a biological hypothyroidism (mean TSH value 11.87  3.78 mIU/L) which occurred on average 5.6 months after surgery. No patient received suppressive doses of L-T4. TSH values are detailed in Table 2. Comparison between ‘‘need for post-operative L-T4 therapy’’ and ‘‘no need for post-operative L-T4 therapy’’ is presented in Table 3. Pre-operative TSH level, post-operative TSH level, thyroiditis features on histopathological report were not predictive factors of post-operative hypothyroidism. Presence of multiple nodules in the operated lobe was statistically predictive of post-operative hypothyroidism requiring opotherapy: 100% of patients had multiple nodules in the ‘‘need for postoperative L-T4 therapy’’ group against 18% in the ‘‘no need for post-operative L-T4 therapy’’ (p = 0.027). 4. Discussion Publications dealing with nodular recurrence rate after partial thyroid surgery in adults reported values ranging from 7.2% [10] to 60.6% [11]. We observed high levels of heterogeneity between studies that explains this variability and makes comparison difficult. Some reports only focused on solitary nodules [5,12], some on unilateral multi nodular goiters (MNG) [4,13], others, like ours, on both pathologies [11,14]. Depending on the study, the rate of patients who had post-operative ultrasound was different: 100% for Bellantone et al. [14] which is equivalent to what is reported in our present study, 30% for Bourguignat et al. [15], 21% for Niepomniszcze et al. [12]. Altogether, this could lead to an underestimation of recurrence in cases of small nonpalpable nodules. In addition, the definition of recurrence differs between authors, some only considering the increase in volume of the remaining thyroid tissue [16,17], others as us based on the

presence of nodules [18,19]. Finally, the follow-up periods vary from one study to another, ranging from 12 months [16] to 10 years [17]. Nevertheless, common risk factors of recurrence in adults are described in the literature, that we tried to highlight in our pediatric population. It is admitted that thyroid diseases in general have a multifactorial origin, under the influence of genetic (family history) and endogenous (age, gender) factors [20]. Family history of MNG is considered a risk factor for developing nodules [21,22]. Nodular thyroid disease is more common in female patients, including in the pediatric population [23]. There also seems to be an association between gender and nodular recurrence [14,24]. In our study though, as well as that of Marchesi et al. [5], female sex was not statistically associated with a greater risk of recurrence. Age at diagnosis also have an influence on nodular recurrence in adults. It is considered that young age is correlated with a higher recurrence rate [21,25], although this correlation is not reported by all authors [13–15]. In our study, patients with recurrence were significantly younger, with a determining age of 14. In our series as in several others [11,14,17,21], existence of multiples nodules appears to be a factor contributing to recurrence, compared to the presence of a single nodule. It is logical to think that ethiopathological origin of nodular disease affects the evolution of the remaining lobe [12]; for example, an isolated adenomatous nodule would essentially have a monoclonal origin, while a MNG is more likely to have a polyclonal origin [26,27]. On a histological basis, Marchesi et al. [5] consider that follicular adenoma is an isolated pathology within a healthy gland, while nodular hyperplasia, rather found in MNG, is a condition of the entire gland. They found a greater risk of recurrence associated with nodular hyperplasia, though without reaching statistical significance threshold. This was also the case in our study. This assumption is to be taken carefully, as not all MNG have the same histology, and/or are driven by clonality. Ultimately, Marchesi’s hypothesis does not allow a better pre-operative assessment of nodular recurrence risk, first because the two types of lesions may coexist in the same thyroid gland [12], secondly because it is only possible to precisely differentiate them by histological analysis, which means post-surgery.

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Several authors have hypothesized that post-operative L-T4 therapy could hinder MNG recurrence, by retro negative control on the production of TSH. However, this hypothesis is controversial; in a literature review of 2008, Moalem et al. [22] assessed that approximately 50% of studies on the subject support this hypothesis, but with sometimes questionable methodology. L-T4 was used with non-suppressive doses [13,14], or with suppressive doses [12,19,24]. However, this efficacy could be subjected to certain conditions depending on the study: only in case of iodine deficiency [13,19], only in patients with a history of neck irradiation in childhood [24], rather for MNG than for solitary nodules [19]. One hypothesis that could explain this variable efficiency is the empowerment of some nodules toward hypothalamic pituitary axis regulation [22]. Besides, significant side effects of suppressive doses treatment have been described: ischemic heart decompensation [28], atrial fibrillation in the elderly [29], acceleration of bone loss in postmenopausal women [30]. In a prospective randomized study, Hegedus et al. [17] did not find any efficacy of post-operative L-T4 therapy in this indication. To prevent MNG recurrence in areas of endemic goiter, they suggest iodine supplementation rather than L-T4 therapy. Finally, they consider that the hypothetical preventive effect on nodular recurrence does not justify the potential side effects of suppressive therapy. In our study, substitutive L-T4 therapy does not have any influence on nodular recurrence. Therefore, in children and adolescents, given the unproven efficacy, and potential morbidity, it appears more reasonable to use post-operative hormonal treatment in replacement indication only, in the case of proven biological hypothyroidism. This does not exclude a possible preventive effect on the occurrence of new nodules on the remaining thyroid tissue. This strategy is also recommended in adults by McHenry et al. [7]. The rate of post-operative hypothyroidism after hemi thyroidectomy in adults found in literature varies from 10.9% [31] to 42.6% [32]. In 2012, a meta-analysis of Verloop et al. [33] reported that 1 in 5 patients would develop hypothyroidism after hemi thyroidectomy. These data are close to our results in children. Faced with a post-operative symptomatic hypothyroidism, the indication of hormone replacement therapy is formal, regardless of age. It is questionable against patients with biological hypothyroidism but clinically asymptomatic [7]. However, in children, the influence of thyroid hormones on growth, bone maturation and cognitive development must be taken into consideration. In a review of the literature concerning asymptomatic hypothyroidism in children, De Luca et al. [34] discussed L-T4 treatment indications. They don’t recommend hormone replacement if TSH remains between 5 and 10 IU/L, unless there exists an underlying disease: goiter, nodules and positive thyroid antibodies. Indeed, these are risk factors for thyroid dysfunction. Therefore, the authors propose to introduce a replacement therapy in any children with a TSH greater than 10 IU/L, and in patients with a TSH between 5 and 10 IU/L but with thyroid underlying disease, which is the strategy we follow in our centre. As for nodular recurrence, we wanted to highlight in our pediatric population the risk factors of post-operative hypothyroidism described in the adult literature. A high pre-operative TSH is the most frequently found risk factor [7,8,31,32,35,36], likely reflecting an already precarious thyroid function. In our study, this report was not significant. However, given the limited number of patients, our results can be questioned, the comparison of limited groups of patients exposing us to the risk of sampling fluctuation. It is therefore likely that this risk factor, universally accepted in the adult, is also in children. Ertek et al. [37] showed that high postoperative TSH also was a predictive factor of hypothyroidism. In our series, 2 months post-operative TSH tended to be higher in

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patients who developed hypothyroidism, but this report was not significant. As in adult [8,38], presence of multiple nodules was statistically associated with the occurrence of post-operative hypothyroidism in our study. This is consistent with the hypothesis that nodular hyperplasia found in MNG is a condition of the entire gland. Lymphocytic infiltration of the thyroid tissue is a risk factor that appears in several publications [8,12,31,32,39]. This pathological data is closely correlated with the presence of serum thyroid antibodies [32]. Our results are limited to support this hypothesis, as only 1 of our patients had lymphocytic thyroiditis, and developed hypothyroidism. Furthermore, the determination of serum antibodies had not been realized systematically for our patients. Finally, there is an influence of the remaining thyroid volume on post-operative function [10,35,36]. Moon et al. [36] showed that it was an independent risk factor for occurrence but also severity of post-operative hypothyroidism. For Mann et al. [10], a remaining thyroid volume of 7.3 mL is needed for good thyroid function; therefore they call for hormone replacement therapy when the remaining volume is less than 10 mL, which can be predicted by an equation based on pre-operative ultrasound measurements [36]. Our study can be criticized on this particular point, since these measures had not been made, due to the achievement of ultrasound in different centres, and the lack of standardized reports. MNG standard surgical treatment is total thyroidectomy [22]. However, several authors propose to achieve a LI if MNG is limited to one thyroid lobe [4,11,40], including in children [2]. Arguments in favour of TT are a lower nodular recurrence rate [22,40], a rate of permanent surgical complications (recurrent laryngeal nerve paralysis, hypoparathyroidism) not higher if in experienced hands [4,22], and surgical difficulties increased if LI was performed first with need for further completion thyroidectomy [22]. Arguments in favour of LI are a lower rate of transitory surgical complications (recurrent laryngeal nerve paralysis, hypocalcaemia, hematoma) [4,22,40], a low rate of completion thyroidectomy [11], and requirement for a life hormone replacement therapy if TT. We chose to perform a nodule resection in four patients, for which the nodule was easily accessible. The aim was to leave the greatest remaining thyroid volume possible, but this strategy can be criticized, as it can lead to a greater blood loss, and greater surgical difficulties if any further surgery is necessary. In our study, despite a rate of nodular recurrence of 27.8%, only 5.5% of patients required completion thyroidectomy, without further complication, and 78.6% of patients required no replacement therapy. These data support partial thyroid surgery, especially as they relate to a pediatric population. Main limitations of this study are its retrospective nature, responsible for some missing data (TSH results, thyroid volume measurements), and its small sample size, due to the rarity of this pathology in a pediatric population. 5. Conclusion In this children and adolescents population, after performing LI or NR, the remaining thyroid tissue remains free of nodules in 72.2% of cases, and does not require further surgery in 94.5% of cases. Risk factors for nodular recurrence are age under 14 years, and the presence of multiple nodules; post-operative L-T4 therapy has no preventive effect on the occurrence of new nodules. After LI, biological hypothyroidism appears in 21.4% of cases; we recommend in this case a systematic substitutive therapy. The only risk factor for post-operative hypothyroidism identified in this study is the presence of multiple nodules. These findings do not significantly differ from an adult population. However, these data

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ought to be confirmed by prospective pediatric studies of larger cohorts. Faced with unilateral benign nodular disease in children and adolescents, we recommend performing a lobectomy– isthmusectomy rather than a first-line total thyroidectomy. Disclosure of interest None. References [1] M. Niedziela, Pathogenesis: diagnosis and management of thyroid nodules in children, Endocr. Relat. Cancer 13 (2) (2006) 427–453. [2] B. Millman, P.K. Pellitteri, Nodular thyroid disease in children and adolescents, Otolaryngol. Head Neck Surg. 116 (6 Pt 1) (1997) 604–609. [3] J. Astl, et al., Thyroid surgery in children and adolescents, Int. J. Pediatr. Otorhinolaryngol. 68 (10) (2004) 1273–1278. [4] P.S. Bauer, et al., Unilateral thyroidectomy for the treatment of benign multinodular goiter, J. Surg. Res. 184 (1) (2013) 514–518. [5] M. Marchesi, et al., High rate of recurrence after lobectomy for solitary thyroid nodule, Eur. J. Surg. 168 (7) (2002) 397–400. [6] T. Zelmanovitz, et al., Analysis of the factors associated with recurrence of postthyroidectomy goiter, Rev. Assoc. Med. Bras. 41 (2) (1995) 86–90. [7] C.R. McHenry, S.J. Slusarczyk, Hypothyroidisim following hemithyroidectomy: incidence, risk factors, and management, Surgery 128 (6) (2000) 994–998. [8] F.R. Miller, et al., Risk factors for the development of hypothyroidism after hemithyroidectomy, Arch. Otolaryngol. Head Neck Surg. 132 (1) (2006) 36–38. [9] M. Akkari, et al., Thyroid surgery in children and adolescents: a series of 65 cases, Eur Ann Otorhinolaryngol Head Neck Dis. (2014), http://dx.doi.org/10.1016/ j.anorl.2013.11.009, pii: S1879-7296(14)00088-X. [10] B. Mann, P. Schmale, W. Stremmel, Thyroid morphology and function after surgical treatment of thyroid diseases, Exp. Clin. Endocrinol. Diabetes 104 (3) (1996) 271–277. [11] G. Yetkin, et al., Does unilateral lobectomy suffice to manage unilateral nontoxic goiter? Endocr. Pract. 16 (1) (2010) 36–41. [12] H. Niepomniszcze, et al., Long-term follow-up of contralateral lobe in patients hemithyroidectomized for solitary follicular adenoma, Clin. Endocrinol. (Oxf) 55 (4) (2001) 509–513. [13] M. Barczynski, et al., Five-year follow-up of a randomized clinical trial of unilateral thyroid lobectomy with or without postoperative levothyroxine treatment, World J. Surg. 34 (6) (2010) 1232–1238. [14] R. Bellantone, et al., Predictive factors for recurrence after thyroid lobectomy for unilateral non-toxic goiter in an endemic area: results of a multivariate analysis, Surgery 136 (6) (2004) 1247–1251. [15] E. Bourguignat, et al., Conditions of the remaining thyroid tissue after partial thyroidectomy, Ann. Otolaryngol. Chir. Cervicofac. 112 (7) (1995) 330–335. [16] J. Berglund, et al., Rapid increase in volume of the remnant after hemithyroidectomy does not correlate with serum concentration of thyroid stimulating hormone, Eur. J. Surg. 164 (4) (1998) 257–262. [17] L. Hegedus, B. Nygaard, J.M. Hansen, Is routine thyroxine treatment to hinder postoperative recurrence of nontoxic goiter justified? J. Clin. Endocrinol. Metab. 84 (2) (1999) 756–760. [18] A. Berghout, et al., The long-term outcome of thyroidectomy for sporadic nontoxic goitre, Clin. Endocrinol. (Oxf) 31 (2) (1989) 193–199.

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Nodular recurrence and hypothyroidism following partial thyroidectomy for benign nodular thyroid disease in children and adolescents.

Diagnostic and therapeutic processing of a thyroid nodule in children and adolescents may require lobectomy-isthmusectomy (LI) or nodule-resection (NR...
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