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Annales d'Endocrinologie
Volume 75, n° 3
pages 141-147 (juillet 2014)
Doi : 10.1016/j.ando.2014.02.001
Pyramidal lobe decreases endogenous TSH stimulation without impact on radio-iodine therapy outcome in patients with differentiated thyroid cancer
Le lobe pyramidal diminue la stimulation de la TSH endogène sans impact sur le résultat d’un traitement à l’iode radioactif chez les patients atteints de cancer différencié de la thyroïde
 

Nadia Sawicka-Gutaj , Aleksandra Klimowicz , Jerzy Sowinski , Robert Oleksa , Maria Gryczynska , Anna Wyszomirska , Agata Czarnywojtek , Marek Ruchala
 Department of Endocrinology, Metabolism and Internal Medicine, Poznan University of Medical Sciences, 49, Przybyszewskiego Street, 60355 Poznan, Poland 

Corresponding author.
Abstract
Objectives

The aim of the study was to assess the frequency of pyramidal lobe (PL) detected in iodine-131 (I-131) scans of thyroid bed in patients after thyroidectomy for differentiated thyroid cancer (DTC) and to investigate influence of PL on endogenous thyrotropin (TSH) stimulation as well as on the effects of the radio-iodine ablation in one-year follow-up.

Patients and methods

This study was designed as a retrospective analysis of 302 radio-iodine neck scans of patients thyroidectomized due to DTC. The study population was selected from patients with PL detected in thyroid bed scintigraphy. Patients without PL were included to the control group. The study and the control groups did not differ in age, sex of patients, histological type and stage of the DTC.

Results

Pyramidal lobes were found in 30.5% of all patients. Patients in the study group underwent repeat surgery more often than controls without PL. Preablative TSH level in patients with PL was statistically lower than in the control group, in contrast to free thyroid hormones, which were higher in patients with PL. Preablative and postablative TSH-stimulated thyroglobulin (Tg) and antibodies against thyroglobulin (TgAbs) were measured in both groups, and comparison did not reveal differences. Moreover, for the per-patient analysis, sites of uptake in whole body scintigraphy performed 1 year after radio-iodine remnant ablation (RRA) did not differ between the study and the control groups.

Conclusion

Pyramidal lobe decreases endogenous TSH stimulation without impact on radio-iodine therapy outcome in patients with DTC.

The full text of this article is available in PDF format.
Résumé
Objectifs

L’objectif de l’étude était d’évaluer la fréquence du lobe pyramidal (LP) détecté lors de scanners à l’iode-131 (I-131) du lit thyroïdien chez des patients ayant subi une thyroïdectomie pour cancer différencié de la thyroïde (CDT), puis d’étudier l’influence du LP sur la thyrotropine endogène (TSH) aussi bien que sur les effets de l’ablation à l’iode radioactif à une année de suivi.

Patients et méthodes

Cette étude est une analyse rétrospective de 302 scanners du cou à l’iode radioactif de patients thyroïdectomisés pour CDT. La population d’étude a été choisie parmi les patients atteints de PL diagnostiqués lors d’une scintigraphie du lit thyroïdien. Les patients sans PL ont été inclus dans le groupe contrôle. Les groupes d’étude et contrôle étaient appariés pour l’âge, le sexe, le type histologique et le stade du CDT.

Résultats

Des lobes pyramidaux ont été retrouvés chez 30,5 % de la totalité des patients. Les patients du groupe d’étude ont subi une chirurgie répétée plus souvent que les contrôles sans PL. Les taux préablatifs de TSH chez des patients atteints de PL étaient statistiquement plus faibles que dans le groupe contrôle, à la différence des hormones thyroïdiennes libres, plus élevées chez les patients atteints de PL. La thyroglobuline (Tg) stimulée préablative et postablative (Tg) et les anticorps anti-thyroglobuline (TgAbs) ont été mesurés dans les deux groupes, et aucune difference significative n’a été relevée. En outre, s’agissant de l’analyse par patient, les sites de fixation dans l’ensemble de la scintigraphie du corps effectués 1 an après l’ablation à l’iode radioactif ne différaient pas entre les groupes d’étude et contrôle.

Conclusion

Le lobe pyramidal diminue la stimulation de la TSH endogène sans impact sur les résultats du traitement à l’iode radioactif chez les patients avec CDT.

The full text of this article is available in PDF format.

Keywords : Thyroid gland, Pyramidal lobe, Cancer of thyroid, Thyroidectomy, Scintigraphy

Mots clés : Glande thyroïde, Lobe pyramidal, Cancer de la thyroïde, Thyroïdectomie, Scintigraphie


Introduction

Since thyroid gland diseases are the most frequent endocrine disorders, thyroid anatomy, morphology, variations are an object of interest of many scientists and clinicians. Pyramidal lobe (PL) was firstly described by Lalouette in 1749. This accessory thyroid tissue is an embryological remnant of the thyroglossal duct. However, variations and occurrence of PL are still under the debate. Many investigations including cadaver, surgical or imaging studies provided contradictory data concerning prevalence and features of PL.

Thyroidectomy is the most common surgical intervention in the head and neck region, therefore the knowledge about anatomical variations of the thyroid gland is relevant. Firstly, it increases the safety of the operation. Secondly, it may improve the efficacy of such interventions and may lead to total removal of thyroid tissue, what is especially important in patients with differentiated thyroid cancer (DTC) or Graves’ disease (GD) [1, 2]. However, data concerning frequency of PL still remains unclear. One may suggest, that the most reliable observations regarding anatomy of thyroid gland were made through cadaver studies. In such investigations, cadavers free from thyroid diseases were selected. However, prevalence of anatomical variations and developmental anomalies of thyroid gland reported in many autopsy studies has not been clearly defined yet. The frequency of PL varies from 28.9% found by Harjeet et al. in North West Indians to more than 60% reported by Blumberg and 76.8% described in the study of 168 Korean cadavers [3, 4, 5]. The prevalence of PL in randomly selected patients who underwent computed tomography of the neck reported in a recent multicenter study ranged from 28% to 55% [6].

Scintigraphy provides information about both structure and function of thyroid gland. Hence, occurrence of PL in scintigraphic visualization depends on functional disorders of thyroid [7]. Wahl et al. showed that PL is observed with increased frequency in scintigrams of subjects with GD, even in patients already treated with anti-thyroid drugs, as compared with patients with toxic nodular goiter [7]. Moreover, pyramidal lobes seem to be more specifically reported in scintigraphy with I-123, which is organified in thyroid gland, than with Tc-99m [8].

Age, gender, race, region, where the study was carried out may affect these results. Due to physiological atrophy of PL, it may be less prevalent in older subjects. There is no agreement, if it is found more frequently in females as compared with males. Some studies reported similar prevalence of PL for both genders [9, 10, 11]. In contrast, Rande et al. found PL only in male cadavers [12]. Data concerning size and length of PL is inconclusive. Some authors observed that PL was longer in females [9, 11].

Moreover, highly variable positions of the PL origin have been reported. Many authors found that most frequently it arose from the isthmus [11, 13]. The others observed that usually it is attached to the left or right lobe [14, 15]. These differences may be caused by the fact that, in some cases, macroscopical observation did not give clear answer, where was the origin of PL.

Since PL is considered as a potentially active thyroid tissue, it may be affected by autoimmune thyroid diseases and thyroid cancers [11]. Moreover, it may be a primary site of malignant disease [11]. Therefore, it should be removed when total thyroidectomy is performed.

The aim of the study was to assess the frequency of PL detected in iodine-131 (I-131) scans of thyroid bed in patients after thyroidectomy for DTC and to investigate influence of PL on the effects of the radio-iodine ablation in one-year follow-up. Moreover, the influence of residual thyroid tissue on endogenous thyrotropin (TSH) stimulation was determined. Furthermore, sensitivity of ultrasound examination (USG) for detection of PL after thyroidectomy was estimated.

Patients and methods

This study was designed as a retrospective analysis of 302 radio-iodine neck scans performed within 24 months in patients thyroidectomized due to DTC. Diagnosis of DTC was based on histological examination. The study population was selected from patients with PL detected in thyroid bed scintigraphy. Patients without PL were included to the control group.

All patients underwent postoperative scanning with diagnostic activities of I-131 (1mCi=37 MBq) to confirm the presence and extent of residual thyroid tissue. Preablative I-131 scans of thyroid bed were performed under endogenous TSH stimulation (achieved by 4-week withdrawal of levothyroxine). Subsequently, all of them were referred for radio-iodine remnant ablation (RRA). Patients underwent postablative I-131 scans 7 days later. Moreover, TSH-stimulated thyroglobulin (Tg) and interfering antibodies against thyroglobulin (TgAbs) were measured. Every patient underwent USG of the neck with assessment of lymph nodes performed by one physician. USG was performed with ALOKA ProSound alpha 7 with 37mm high resolution linear transducer of 5–13MHz frequency. The volume of thyroid tissue remnants was assessed with ellipsoid formula.

The efficacy of RRA was compared between both groups one year later, when all patients were reassessed by whole body scintigraphy (WBS) and by measurement of serum Tg, TgAbs during hypothyroidism.

Scintigraphic images were assessed independently by two experienced specialists in nuclear medicine. The presence of PL was seen as a vertical strip of radionuclide activity extending cephalad from the thyroid bed. The review process included a consensus procedure in case of disagreement. The physicians were blinded to other imaging results. Positive response for treatment was assessed one year after RRA and it was understood as both negative thyroglobulin and negative uptake on WBS.

Despite a National iodine prophylaxis programme based on mandatory iodisation of hausehold salt with 30±10mg KI/kg salt that was introduced in Poland in 1997, according to World Health Organization, Poland is an area with a mild iodine deficiency (median urine iodine excretion 50–99 mcg/L) [16]. Update on iodine status performed by Zimmermann and Andersson also reports Poland as a country with iodine-deficient regions [17].

The study and the control groups did not differ in age and sex of patients, histological type and stage of the DTC.

Statistical analyses were performed using MedCalc for Windows, version 12.1.3.0 (MedCalc Software, Mariakerke, Belgium). Normality was analyzed by D’Agostino-Pearson test. P -value less than 0.05 indicated statistical significance.

Results

Pyramidal lobes were found in 91 scintigraphic images (30.5% of all patients). However, 4 patients did not undergo total thyroidectomy, therefore they were excluded from the further analysis. The study group consisted of 87 patients with pyramidal lobes detected in thyroid bed scan (Table 1). The control group consisted of 60 patients without PL detected in thyroid bed scan who underwent total thyroidectomy for DTC (Table 1).

PL was found in the midline in 51 patients (58.5% of the study group), in 18 (20.7%) patients, the PL was located laterally on the left and similarly in 18 (20.7%) patients, it was found on the right. Patients in the study group underwent repeat surgery more often than controls without PL (P =0.0194, Fisher's exact test). In the study group, 19 (21.8%) patients underwent secondary thyroidectomy. Only 4 of 60 patients (6.7%) in the control group had been thyroidectomized twice. Thyroid resection was performed before thyroid bed scan in every patient.

All subjects achieved TSH level above 30 IU/L required for maximum radio-iodine uptake. Preablative TSH level in patients with PL was statistically lower than in the control group (Table 2, Fig. 1). During reassessment, 1 year after RRA, TSH level of patients from the study group and of controls did not differ. Preablative TSH concentrations in the study group were statistically higher than determined 1 year after the RRA (Table 2). Free thyroid hormones, namely free thyroxine and free triiodothyronine were not routinely tested in all patients. Preablative FT4 level was assessed in 50 patients with PL and in 34 controls, and preablative FT3 was tested in 47 patients with PL and 33 controls. Comparison between the study and the control groups showed higher concentrations of free thyroid hormones in patients with PL (Fig. 2, Fig. 3). During reassessment one year after RRA, free thyroid hormones in the study and in the control groups did not differ.



Fig. 1


Fig. 1. 

Comparison of TSH between the study group (TSH) and controls (TSH-C) during preablative evaluation. Median TSH concentration 67.01 IU/L (IQR=52.60–91.95) and median TSH-C concentration 91.60 IU/L (IQR=65.56–100.00). (U Mann-Whitney test, P =0.0002).

Zoom



Fig. 2


Fig. 2. 

Comparison of FT4 between the study group (FT4) and controls (FT4-C) during preablative evaluation. Median FT4 concentration 2.28pmol/L (IQR=1.64–3.57) and median FT4-C concentration 1.90pmol/L (IQR=1.2–2.47). (U Mann-Whitney test, P =0.0211).

Zoom



Fig. 3


Fig. 3. 

Comparison of FT3 between the study group (FT3) and controls (FT3-C) during preablative evaluation. Median FT3 concentration 1.38pmol/L (IQR=0.88–2.88) and median FT3-C concentration 1.15pmol/L (IQR=0.60–1.37). (U Mann-Whitney test, P =0.0139).

Zoom

RRA was performed with 60 to 150 mCi (2.22 GBq to 5.55 GBq) I-131 adjusted for tumour stage, administered orally, and there was no difference between activities of I-131 used in the study and in the control groups (Table 3).

Preablative and postablative TSH-stimulated Tg and TgAbs were measured in both groups, and comparison did not reveal differences (Fig. 4). Moreover, for the per-patient analysis, sites of uptake in diagnostic WBS performed 1 year after RRA did not differ between the study and the control groups (Table 4). In conclusion, response for therapy assessed one year after RRA was similar in both groups (Table 5). Comparison of Tg, TgAbs, activities of I-131 assessed one year post radio-iodine therapy between patients with PL who underwent secondary operation and those who had only one did not reveal any differences.



Fig. 4


Fig. 4. 

Comparison of thyroglobulin (Tg) and antibodies against thyroglobulin (TgAbs) between the study group and controls. A. Preablative Tg serum concentration and TgAbs titer in the study group (Tg; TgAbs) and in the control group (Tg-C, TgAbs-C). Median Tg concentration 4.56ng/mL (IQR=1.43–9.67) and median Tg-C concentration 3.44ng/mL (IQR=0.82–8.27). (U Mann-Whitney test, P =0.1352). Median TgAbs-1 titer 19 IU/L (IQR=10–49.75) and medianTgAbs-C1 titer 19 IU/L (IQR=13–38.5). (U Mann-Whitney test, P =0.9778). B. Postablative Tg serum concentration and TgAbs titers in the study group (Tg-1) and in the control group (Tg-C1). Median Tg-1 concentration 0.14ng/mL (IQR=0.1–0.78) and median Tg-C1 concentration 0.27ng/mL (IQR=0.1–1.48). (U Mann-Whitney test, P =0.7436). Median TgAbs-1 titer 12 IU/L (IQR=0–22.75) and medianTgAbs-C1 titer 15 IU/L (IQR=11–24). (U Mann-Whitney test, P =0.0932).

Zoom

Sensitivity of the ultrasound examination for the detection of PL after thyroidectomy was 31%.

Discussion

Data regarding the frequency of pyramidal lobes left after total thyroidectomy is limited. Recent autopsy investigations revealed the presence of PL in up to 76.8% of subjects (Table 6). We have reported that it was found in preablative I-131 scans in 30.5% of patients who underwent thyroidectomy due to DTC. As was mentioned, in general, scintigraphic imaging of thyroid gland does not give reliable information concerning the prevalence of PL, because its visualization depends on functional state of this endocrine gland (Table 7). Some authors suggest that PL is more reliably visualized on radio-iodine scans as compared with pertechnetate, which is pseudohalide and it is trapped by thyroid gland only temporarily, because it is not organified [7, 8].

On the contrary, in thyroidectomized patients, preablative I-131 scans of thyroid bed have relatively high sensitivity in detection of remnant thyroid tissue. However, the main limitation of our study is the possibility of false interpretation as to what constitutes the PL. The detection of radio-iodine uptake on preablative scans could also indicate for other thyroid duct remnants including thyroid duct cysts (TDC). To decrease the magnitude of this bias on our findings, the PL was defined as a vertical strip of radioactivity extending upwards from thyroid bed and the review process was based on the consensus procedure. Moreover, the prevalence of TDC is much lower than the prevalence of PL, and is estimated for 7% of population. Additionally, TDC is found predominantly in children and the occurrence of TDC in adults older than 60 years is estimated for 0.6% [24, 25]. Therefore, the risk of potential misdiagnose is not thought to be significant in this study.

Besides the necessity of excision of PL during total thyroidectomy, it seems that it was not resected in majority of patients. Removal of PL, as a normal component of thyroid gland, is of great importance in surgery of patients with DTC. Significant volume of remnants of thyroid tissue leads to increased level of circulating thyroglobulin that interferes with further follow-up, and, what is the most important, it may lead to a higher rate of recurrence of malignancy. Interestingly, patients with missed pyramidal lobes revealed in scintigraphic visualization had undergone secondary operation more often than those who had total removal of thyroid gland in primary operation. One may suggest that, increased risk of postoperative complications associated with secondary thyroidectomy, namely hypoparathyroidism or vocal cord paresis, together with adhesions, may lead a surgeon to be more cautious in exploration of the visceral compartment of the neck. Moreover, since diameters of PL are relatively low, its detection during thyroid surgery appears to be difficult. On the other hand, it was recognized that PL undergoes hypertrophy if it is not removed during thyroidectomy and if the postoperative treatment with L-thyroxine is insufficient to suppress TSH. In addition, PL may be involved in DTC, rarely it is a primary site of papillary or follicular thyroid cancers [26, 27]. Studies concerning response for treatment of DTC arising from PL are lacking, however, recently published analysis of cancer in TDC showed more aggressive features such as multifocality, concomitant cancer in thyroid gland and lymph node involvement [28]. Choi et al. underlined the necessity of careful thyroid and neck lymph nodes evaluation in patients with suspicion of TDC cancer [29]. Moreover, Dzodic et al. suggested that total thyroidectomy should be mandatory in all patients with carcinoma arising from TDC [30]. Undoubtedly, patients with DTC require successful thyroid remnant ablation at the early stage of treatment.

The effectiveness of radio-iodine therapy of patients with DTC is based on sufficiently elevated TSH above 30 IU/L leading to increase of expression of NIS (natrium iodine symporter), and to stimulate the uptake of administred I-131 by both thyroid tissue remnants and DTC. In our study, all patients with PL achieved the preablative TSH concentration above 30 IU/L, however, it was lower than in controls. The positive correlation between the effective radiation dose and the outcome of therapy in patients with DTC and metastases is established [31, 32]. Moreover, significant positive correlation was revealed between TSH concentration and effective half-life of I-131 in DTC patients during RRA [33]. Since the serum level of TSH plays a crucial role in the efficacy of RRA, one may suggest that response for therapy is worse in patients with PL because of lower TSH concentration. However, we did not establish the negative influence of PL on effects of radio-iodine ablation in one-year follow-up defined as both of negative WBS and undetectable serum level of thyroglobulin. The ablation protocol of patients with DTC in our department is based on empirical activities of I-131 adjusted for tumour stage and 60 mCi is the lowest prescribed activity. Therefore, the lack of influence of PL on effectiveness of ablation may be caused by the high-dose ablation regimen prescribed in all patients with DTC. The best fixed dose of I-131 for effective thyroid ablation is still under debate and it is not an object of our study. Recently published meta-analysis performed by Cheng et al. shown that low dose of I-131 is sufficient for thyroid remnant ablation as compared with 3700 MBq [34]. The patients included into the meta-analysis had undergone total or near-total thyroidectomy, therefore these results cannot be extrapolated to our population of patients with pyramidal lobes.

To the best of our knowledge, the sensitivity of PL detection in ultrasound examination has not been reported. Therefore, it is not possible to compare our results with other investigations. Moreover, PL is considered as a rare finding in ultrasound examination [35].

Since iodine deficiency causes a goitre, it may also lead to PL enlargement [36]. Furthermore, in subjects with latent hypothyroidism and iodine deficiency, vestiges of thyroglossal tract were found more frequently [7]. However, studies evaluating direct association between iodine deficiency and incidence of PL are lacking.

To summarize, PL was found in almost one third of patients who had undergone thyroidectomy due to DTC. PL was hormonally active tissue and therefore caused the lower TSH level without negative effect on the radio-iodine therapy outcome. However, it should be underlined that in our study, the successful remnant ablation was assessed in relatively short time, and the studies on the influence of PL on long-term relapse rate are needed.

Disclosure of interest

The authors declare that they have no conflicts of interest concerning this article.


Acknowledgement

This study was supported by a Grant from Poznan University of Medical Sciences, Poland. (Grant No. 502-14-02221355-99664).

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