Is radioiodine ablation with 30 mCi 131I necessary in low-risk thyroid cancer patients? Results from a long-term follow-up prospective study.

doi:10.21203/rs.3.rs-2359357/v1

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Is radioiodine ablation with 30 mCi 131I necessary in low-risk thyroid cancer patients? Results from a long-term follow-up prospective study.

https://doi.org/10.21203/rs.3.rs-2359357/v1

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Journal Publication

published 29 Mar, 2023

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In patients with low-risk differentiated thyroid cancer (DTC), remnant ablation with radioiodine (RA) after total thyroidectomy (TT) is controversial. No benefits have been demonstrated in terms of mortality or disease-free survival. Recent evidence found that RA did not improve mid-term outcomes.

Purpose: to evaluate initial response to treatment and long-term follow-up status in low-risk DTC patients after TT vs. TT+RA.

Methods: prospective multicenter non-randomized study; 174 low-risk DTC that underwent TT were recruited and were divided in two groups according to RA (87 ablated and 87 non-ablated). Response to treatment was evaluated between 6-18 months after thyroidectomy and at the end of follow-up with thyroglobulin, anti-thyroglobulin antibodies levels and neck ultrasonography.

Results: baseline characteristics of both groups were similar. Ablated patients: median age 45.5 years, 84% females, 95.4% papillary thyroid carcinoma (PTC), mean tumor size 16mm; non-ablated: median age 45 years, 88.5% females, 96.6% PTC, mean tumor size 14 mm. Response to initial treatment was similar between both groups, with less than 2% of structural incomplete response. Final status was evaluated in 139 cases after a median follow-up of 60 months. Among ablated patients, 82.8% had no evidence of disease (NED), 12% had an indeterminate response (IR) and 5% a biochemical incomplete response (BIR). Non-ablated patients had NED in 90%, IR in 8.7% and BIR in 1.2%. No statistical difference was found between groups (p=0.29). No patient had evidence of structural disease at the end of follow-up.

Conclusions:our findings support the recommendation against routine RA in low-risk DTC patients.

differentiated thyroid cancer

low-risk patients

remnant ablation

response to treatment

The therapeutic approach of patients with differentiated thyroid cancer (DTC) is currently individualized according to the risk of recurrence. As stated by the initial risk stratification system of the American Thyroid Association (ATA), patients are considered to be at low risk of recurrence when no local invasion, vascular invasion or metastases are found, all macroscopic tumor has been resected, the tumor does not have aggressive histology (i.e., tall cell), and no clinically involved lymph node or < 5 pathologic N1 micrometastases (< 0,2 cm in largest dimension) are detected [1]. Most of these patients are included in the low-risk of recurrence category [2–3]. Structural incomplete responses are observed in 3 to 7% of low-risk patients who are treated with total thyroidectomy and radioiodine ablation [4–8]. Benefit of remnant ablation (RA) in low-risk patients is uncertain [9–10]. In retrospective studies, RA did not demonstrate to reduce mortality or to improve disease-free survival [11]. A recent prospective multicentric study found no differences in outcomes of DTC patients with tumors < 2 cm, no lymph node metastases and no aggressive histology treated with total thyroidectomy alone vs. thyroidectomy and RA [12]. While RA may facilitate detection of persistent/recurrent disease during follow-up, some studies argue that in non-ablated patients with low/undetectable thyroglobulin levels and negative findings on neck ultrasound, the probability of recurrence is < 2% [13–14].

In order to determine the outcomes of low-risk DTC patients submitted to low-dose RA compared to those who do not receive remnant ablation, we performed a prospective multicentric study aiming a) to assess response to initial therapy, and b) to evaluate long-term follow-up status in both groups of patients.

This was a prospective multicenter, non-randomized study that included patients from fourteen centers of Buenos Aires City. A total of 174 patients were consecutively recruited between June 2014 and May 2015, with last assessment of status in March 2021. The eligibility criteria comprised: a) diagnosis of low risk of recurrence DTC according to the modified 2015 ATA risk stratification system [1]; b) age older than 17 years; c) total thyroidectomy as initial surgery; d) follow-up of at least 24 months to define the initial response to treatment. Exclusion criteria included patients: a) with unifocal microcarcinomas; c) with intermediate risk of recurrence (aggressive histology, vascular invasion, clinical node involvement or > 5 lymph nodes involved of 0.2 cm; d) with high risk of recurrence; e) in whom the extent of surgery could not be determined.

Initial treatment

As previously stated, all patients underwent total thyroidectomy. Therapeutic central lymph node dissection was performed if there was evidence of nodal involvement. Prophylactic central lymph node dissection was performed according to protocols of each participating center. Decision whether to perform radioactive remnant ablation was made in each center according to their usual practices. In case of ablation, the radioactive iodine activity administered was 30 mCi. Preparation for remnant ablation included thyroid hormone withdrawal or recombinant human TSH (rh TSH) injection (0.9 mg administered intramuscularly in two consecutive days). The methodology was selected in agreement with patients’ preferences. Low iodine diet was indicated before ablation. Pre-ablation serum thyrotropin (TSH) level > 50 mIU/L, thyroglobulin (Tg) and thyroglobulin-antibodies (TgAb) levels were obtained in all patients and post-dose whole-body scan was performed within one week after ablation.

Follow-up

After initial treatment, levothyroxine (LT4) replacement therapy was adjusted to maintain a TSH level < 2 mIU/l. Patients were followed up by clinical examination, neck ultrasound and measurement of Tg and TgAb under LT4 at intervals of 6 − 12 months.

Response to treatment was evaluated between 6–18 months after thyroidectomy and at the end of follow-up according to the criteria proposed by the modified 2015 American Thyroid Association guidelines in ablated patients [1], and according to the classification proposed by Momesso et al. in non-ablated patients [15].

Serum Tg and TgAb were assessed with a commercial immunometric assay available in each participating center, and the same assay was used throughout a patient’s follow-up.

The study protocol was approved by every hospital independent ethics committee.

Statistical analysis

Continuous variables are expressed as mean ± standard deviation, or median and ranges. Categorical variables are shown as percentages. Categorical variables were compared using a chi-squared test or Fisher’s exact test, and continuous variables using Mann Whitney test. All data were analyzed using Statistical Package for Social Sciences (SPSS) version 21.0 software (SPSS Inc., Chicago, IL, United States); any p value < 0.05 was regarded as statistically significant.

Enrollment and basal characteristics of the study population are shown in Fig. 1 and Table 1. Most patients were women; median age was 45 years. Papillary thyroid cancer was the most frequent cancer histotype. Ablated and non-ablated patients displayed similar clinicopathological characteristics. Response to initial therapy was assessed in 161 of 174 included patients (92.5%); long-term follow-up data (> 24 months) was available in 139 of 174 patients (86.3%). Median follow-up was 60 months (range: 26–91 months).

Table 1

Characteristics of 174 patients with low-risk differentiated thyroid cancer included in the study
	RA (n = 87)	No RA (n = 87)	p
Gender n (%) Female Male	73 (84) 14 (16)	77 (88.5) 10 (11.5)	0.511
Age (years) Mean ± SD Median (range)	46.8 ± 15.01 45.5 (17–76)	47.5 ± 14.6 45 (17–90)	0.755
Histology n (%) Papillary TC, classical subtype Papillary TC, follicular subtype Follicular TC Papillary TC, other subtype	59 (68) 22 (25) 4 (4.6) 2 (2.4)	66 (75.9) 12 (13.8) 3 (3.4) 6 (6.9)	0.149
Primary tumor diameter (mm)	16 ± 6.7	14.03 ± 7.2	0.063
Bilaterality and multifocality n (%) Bilaterality Multifocality	18 (20.4) 28 (29.5)	24 (27.6) 29 (33.3)	0.292 0.872
Lymphocytic thyroiditis on surgical specimen n (%)	25 (28.4)	33 (37.9)	0.201
Minimal extrathyroidal extension n (%)	12 (13.8)	8 (9.2)	0.477
Positive TgAb n (%)	18 (20.4)	20 (22.9)	0.855
Lymphadenectomy n (%) No Central Central and lateral	55 (63.2) 30 (34.5) 2 (2.3)	55 (63.2) 32 (36.8) -	0.356
Primary tumor (T) n (%) T1 T2	71 (81.6) 16 (18.4)	79 (90.8) 8 (9.2)	0.123
Regional lymph nodes (N) n (%) N0/Nx N1a	72 (82.7) 15 (17.3)	80 (91.9) 7 (8.1)	0.109
Staging (AJCC/UICC) 8º edition n (%) I II	83 (95.4) 4 (4.6)	85 (97.7) 2 (2.3)	0.682

Response to initial treatment is shown in Fig. 2. Clinicopathological characteristics of the patients evaluated at the end of follow-up are shown in Table 2. Final status is shown in Fig. 3. Again, both groups displayed similar characteristics. Three patients with structural incomplete response on assessment to initial therapy were submitted to surgery; two of them were rendered free of disease and the other one had an indeterminate response to treatment.

Table 2

Characteristics of low-risk thyroid cancer patients with long term follow-up (median > 59 months in both groups)
	RA (n = 58)	No RA (n = 81)	p
Gender n (%) Female Male	48 (82.8) 10 (17.2)	71 (87.7) 10 (12.3)	0.46
Age at diagnosis (years) Mean ± SD Median (range)	49 ± 15.14 50 (17–76)	47,8 ± 15.07 47 (17–90)	0.38
Histology n (%) Papillary TC Follicular TC Papillary TC, other subtype	53 (91.4) 3 (5.1) 2 (3.5)	77 (95.1) 3 (3.7) 1 (1.2)	0.611
Primary tumor diameter (mm)	16.4 ± 7.5	14 ± 7.5	0.05
Bilaterality and multifocality n (%) Bilaterality Multifocality	13 (22.4) 15 (25.8)	23 (28.4) 29 (35.8)	0.556 0.268
Lymphocytic thyroiditis on surgical specimen n (%)	15 (25.8)	32 (39.5)	0.14
Minimal extrathyroidal extension n (%)	9 (15.5)	8 (9.9)	0.432
Positive TgAb n (%)	10 (17.2)	19 (23.5)	0.405
Primary tumor (T) n (%) T1 T2	46 (79.3) 12 (20.7)	72 (88.8) 9 (11.2)	0.151
Regional lymph nodes (N) n (%) N0/Nx N1a	48 (82.8) 10 (17.2)	74 (91.4) 7 (8.6)	0.188
Stage TNM (AJCC/UICC) 8º edition n (%) I II	57 (98.3) 1 (1.7)	79 (97.5) 2 (2.5)	1.000
Response to initial treatment n (%) Excellent Indeterminate Incomplete biochemical Incomplete structural	45 (77.7) 10 (17.2) 1 (1.7) 2 (3.4)	71 (87.7) 9 (11.1) 0 (0) 1 (1.2)	0.32
Additional surgical procedure n (%) No Yes	55 (94.9) 3 (5.1)	80 (98.8) 1 (1.2)	0.3
Additional RAI therapy n (%) No Yes	57 (98.3) 1 (1.7)	81 (100) 0 (0)	0.41
Follow-up (months), median (range)	59.5 (26–91)	61 (32–82)	0.128

Of twenty-three patients that had an undetermined response to initial treatment, four were lost to follow-up, 10 persisted with indeterminate response (six due to positive TgAb and four due to low levels of serum Tg), eight switched to excellent response and one had biochemical persistence. At last evaluation, no patient had evidence of structural disease; and no significant differences between ablated and non-ablated patients were found on final status.

In this multicenter prospective study, low-risk DTC patients showed similar outcomes whether low-dose radioiodine ablation was performed or not, underscoring the excellent prognosis of these patients. We did not find structural disease in any of the included patients after a median follow-up of nearly 5 years. Moreover, almost 90% of the cases evolved with no evidence of disease at final follow up. These data are in concordance with the outcomes expected in this subgroup of patients [16–18].

The benefits of not performing RA include avoiding exposure to radiation (which benefits the patient, physicians and the environment), lower costs, eliminating side effects, fewer days of absence from work, and improved quality of life [19–20]. Previously published meta-analyses failed to show advantages of RA in low-risk patients, both in survival and recurrence rates [11].

Although the routine use of adjuvant RA for low- to intermediate-risk DTC is not endorsed by the current ATA guidelines, in European countries, RA is routinely recommended by nuclear medicine specialists for selected low-risk tumors and for most cases with intermediate risk [21]. This reflects not only a lack of consensus between the ATA and European Association of Nuclear Medicine (EANM) with regard to RA for low to intermediate DTCs, but also, a wide variability in RA treatment strategies for DTC, even between recognized experts in the field [22–24]. In this regard, RAI ablation for DTC patients, independently of risk of recurrence, continues to be a widespread medical practice in Argentina, particularly in the private setting. Concerns about the reliability of follow up have been advocated as another reason for performing RA. However, Momesso et al. [15] have established criteria to evaluate non ablated patients. In addition, as most recurrences of papillary thyroid cancer are usually found in cervical lymph nodes, neck ultrasound is a very effective method for ruling out structural disease. In the setting of negative ultrasound, persistently low levels of thyroglobulin are reassuring [25–30]. Nevertheless, optimal thyroglobulin thresholds, interval of measurement and interpretation for clinical management warrant further investigation [31].

Recently, the results of a French randomized prospective multicentric study including 750 low-risk patients evidenced similar rates of events (i.e: abnormal foci of RAI uptake, abnormal neck ultrasound or rising Tg/aTg levels) in patients submitted to RA vs. non-ablated patients. However, this trial assessed a highly selected population, since it excluded patients with metastatic lymph nodes and/or minimal extrathyroidal extension [12]. The present study had a longer time of follow-up, and it included patients with higher-risk features. In this regard, 12.6% of patients with less than 5 metastatic lymph nodes < 0.2 cm and without evidence of extranodal spread were included, a situation that did not have a negative consequence in the final evolution, which expands the current evidence of withholding RAI ablation in thoroughly evaluated patients. Additionally, minimal extrathyroidal extension was present in 11.5% of the patients, and it also had no impact on the final outcome.

The present study has some limitations. As this was a non-randomized study, it is possible that selection bias could occur, nevertheless, both groups displayed similar baseline characteristics. There were some disparities in the number of patients enrolled between institutions that could be related to differences in the proportion of DTC evaluated during the inclusion period.

In conclusion, our findings endorse that systematic radioiodine ablation should not be recommended in low-risk DTC patients.

Acknowledgments

We thank the members of the Thyroid Department of Sociedad Argentina de Endocrinología y Metabolismo:

Abalovich Marcos, Abelleira Erika, Alcaraz Graciela, Bielsky Laila, Brenta Gabriela, Cabezón Carmen, Calabrese M. Cristina, Castro Jozami Lorena, Delfino Laura, Deutsch Susana, Fassi Julieta, Frascaroli Genoveva, Gauna Alicia, Guerra Jorgelina, Jerkovich Fernando, Lowenstein Alicia, Martínez María Paz, Moldes Sofía, Negueruela M. del Carmen, Oneto Adriana, Orlandi Ana María, Parisi Carina, Reyes Adriana, Rosemblit Cynthia, Russo Picasso Fabiana, Saban Melina, Sala Mónica, Schiro Laura, Schnitman Marta, Sklate Rosana, Silva Croome M. del Carmen, Storani María Elena, Zund Santiago, Zunino Anabela.

Funding: The authors declare that no funds, grants or other support were received for conducting this study or preparing this manuscript.

Competing interests: The authors have no relevant financial or non-financial interests to disclose.

Author contribution: All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Verónica Ilera, Inés Califano and Andrea Cavallo. The first draft of the paper was written by Verónica Ilera, Inés Califano and Andrea Cavallo. and all authors commented on previous versions of the paper. All authors read and approved the final manuscript.

Ethics approval: This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of each hospital.

Consent to participate: Informed consent was obtained from participants included in the study.

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Editorial decision: Major Revisions Needed
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You are reading this latest preprint version

Is radioiodine ablation with 30 mCi 131I necessary in low-risk thyroid cancer patients? Results from a long-term follow-up prospective study.

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Abstract

Figures

Introduction

Patients And Methods

Initial treatment

Follow-up

Statistical analysis

Results

Discussion

Declarations

References

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