Skip to main content
Egyptian Journal of Radiology and Nuclear Medicine
Download PDF

Additive value of 18FDG-PET/CT to positive 131I whole body scan in recurrent differentiated thyroid cancer patients with potential influence on treatment strategy: single Egyptian center experience

Egyptian Journal of Radiology and Nuclear Medicine volume 53, Article number: 30 (2022) Cite this article

Abstract

Background

Years ago the utility of of18F-fluorodeoxyglucose-positron emission tomography/computerized tomography (18FDG-PET/CT) in differentiated thyroid cancer was confined mainly to cases with elevated serum thyroglobulin and negative 131I whole body scan. In this study, we try to assess the diagnostic performance of 18FDG-PET/CT in recurrent differentiated thyroid cancer patients with positive 131I whole body scan and in addition to evaluate the impact of 18FDG-PET/CT on the treatment strategy.

Results

The 18FDG PET/CT detected tumor recurrence in 35 (81.3%) patients most of them (91.4%) were in stage IV, while the rest 8.5% was in stage III. No recurrence was detected among patients in stage II and III by 18FDG PET/CT.

Regarding lesion-based analysis, sensitivity of 18FDG-PET/CT was superior to that of 131I post-therapeutic whole body scan (TxWBS) (78.2% vs. 69.4%, respectively), while both modalities had the same specificity (50%). 18FDG-PET/CT changed the treatment plan in 18 (41.6%) patients.

Conclusion

18FDG-PET/CT may be complementary to 131ITxWBS in high-risk DTC with impact on treatment strategy.

Background

Thyroid cancer is a common head and neck malignancy and also it is the most common endocrine tumor in the body [1,2,3]. The incidence of thyroid cancer has rapidly increased in the USA and other developed countries over the past 30 years [4,5,6,7]. From 1975 to 2009 there was a three-fold increase in incidence rates, from 4.9 to 14.3 per 100,000 individuals [6, 8]. Papillary thyroid carcinoma (PTC) and follicular thyroid carcinoma (FTC) are collectively classified as DTC and account for at least 94% of thyroid carcinoma [9]. Both have an excellent prognosis, with a 20 years survival of 90%–95% and 75%, respectively [10]. The postoperative recurrence rate of thyroid cancer is up to 23–30% [11,12,13,14,15,16]. The most effective therapeutic strategies for differentiated thyroid carcinoma (DTC) are thyroid surgery (total or near-total thyroidectomy) followed by iodine-131 (131I) ablation [17]. 131I therapy is not only appropriate for primary tumors but also for lymph node (LN) and distant metastases [18, 19]. However, therapeutic strategies should be more cautiously refined [20].

The role of 18F-fluorodeoxyglucose-positron emission tomography/computerized tomography (18FDG-PET/CT) starts with the development of metastatic diseases, which are not responsive to radioiodine therapy anymore. FDG accumulates in tumor lesions that are missed by iodine scintigraphy [21,22,23]. Loboulleux et al. in their study concluded that in patients with elevated serum Tg level after a total thyroidectomy and a normal post-ablation whole body scan (WBS), 18FDG-PET/CT rather than a post-empiric 131I WBS is preferred for detection of recurrence/metastases [24]. Over the last years, several studies have shown high sensitivity (80–90%) of 18FDG-PET/CT in detecting local or distant recurrences in patients with high thyroglobulin level and negative 131I WBS [25,26,27,28] in addition to recent studies that discuss the role of 18FDG-PET/MR in those patients [29, 30]. However, Piccardo et al. [31] in their study declared impact of 18FDG-PET/CT in changing the management plan in stage IV DTC subgroup with positive 131I WBS. To the best of our knowledge, there is a paucity of studies discussed this issue.

The current study aims to evaluate additive value of 18FDG-PET/CT to patients who were 131I post-therapy whole-body scan (TxWBS) positive for recurrent DTC and to assess how this can influence the treatment strategy.

Methods

The present study enrolled 43 patients selected from 1002 DTC patients referred to nuclear medicine and clinical oncology department from January 2011 to May 2021 by reviewing their medical records, including clinical evaluation, serum Tg and anti-Tg antibodies, neck US, diagnostic 131I WBS, 131I TxWBS, and 18FDG-PET/CT. 18FDG-PET/CT was done at the national cancer institute during the follow-up.

The study design was approved by institutional review board of clinical oncology and nuclear medicine department. Patient consent was not possible because of the retrospective design of the study.

Inclusion criteria: Patients age above 18 years old, with histopathologically proven DTC treated by thyroidectomy and 131I treatment. We selected the patients who done18FDG-PET/CT within 3 months prior to 131I therapy in whom 131I WBS was positive for suspicious locoregional or distant recurrence either clinically or biochemically by elevated Tg serum level in hypothyroid status. The locoregional and distant recurrences were proven pathologically (fine needle aspiration [FNA] cytology or excisional biopsy), or by conventional imaging (neck ultrasound [US], Tc99m MDP bone scan, chest CT and triple phase CT) or by follow-up for at least one year post 18FDG-PET/CT scan to evaluate lesion behavior overtime; stationary or regressive course of the lesion after 131I therapy or progression with time confirms its malignant nature.

Exclusion criteria: Patients with elevated thyroglobulin (Tg) serum level and negative 131ITxWBS or with history of second primary malignancy.

Serum Tg and Tg antibodies measurement: Blood samples were obtained to measure both Tg and Tg antibodies serum levels in all patients in hypothyroid state (thyroid stimulating hormone (TSH) level ≥ 30 mIU/L). Serum Tg level was considered abnormal when its value was higher than 1 ng/ml.

Neck ultrasound (U/S): Neck U/S was performed for all the patients to evaluate the thyroid bed as well as central and lateral cervical nodal compartments. Sonographically suspicious lymph nodes were biopsied for cytology or excised for histopathology. Suspicious criteria for metastases include round shape, hyperechogenicity, microcalcification, hypervascularity, cystic aspect and loss of hilar fat.

CT chest and triple phase CT were done for suspected lung and liver metastases, respectively. CT imaging was acquired by 64 multi-detectors CT scanner. All CT images were interpreted by expert radiologists.

Technetium methylene diphosphonate (Tc99m MDP) scan: 3 h post-injection of 740 Mbq (20 mCi) of Tc99m MDP anterior and posterior whole body planner images were acquired. Abnormal focal tracer uptakes are suspicious of osseous deposits.

131I scans: Both diagnostic and Tx WBS were done in all the patients after hormonal withdrawal for 4 weeks with the TSH serum level ≥ 30 mIU/L. Patients were also instructed to follow a low iodine diet 2 weeks prior to iodine intake. Diagnostic 131I WBS was performed after oral intake of 185 MBq (5 mCi), while 131I TxWBS was done after large dose (100-200 mCi) 5–7 days later. Imaging was done with a dual-headed gamma camera using high-energy collimators. The energy window was set at 15% centered on 364 keV with a 256 × 1024 size with a scan speed of 15 cm/min. The images were evaluated for iodine avid locoregional or distant recurrences. Images were interpreted by two experienced nuclear medicine physicians. Any abnormal focal iodine activity in operative thyroid bed, anatomical sites of lymph nodes or the rest of the body was interpreted as positive result.

18FDG-PET/CT: The scan was done using (PET/CT 710, Discovery; general electric (GE)). All patients were instructed to fast for 4–6 h before injection of 5.2 MBq (0.19 mCi)/kg body weight 18FDG. Blood glucose level was not exceeding 150 mg/dL, 40–60 min post-tracer injection CT was acquired first followed by PET scanning (5–7 bed positions; acquisition time, 2–3 min/bed position). CT without contrast agent was performed with the following parameters: 40 mAs, 130 kv, slice thickness: 2.5 mm, and pitch: 1.5. The CT scans were acquired during breath holding. Patients are scanned in the supine position from skull base to mid-thigh. The CT-data were used for attenuation correction and anatomical localization. Images were reconstructed applying a standard iterative algorithm (ordered-subset expectation maximization). Images were interpreted at a workstation equipped with fusion software that provides multi-planar reformatted images and enables display of the PET, CT and fused PET/CT images. Image interpretation was accomplished by two experienced nuclear medicine physicians. Abnormal FDG uptake was defined as a focal increased uptake higher than that of liver activity at anatomic localizations.

Data analysis was based on patients, organs and lesions. Organs are classified into: thyroid bed, LN (cervical), lung, liver, and bone. Lesions in one lung regardless of their numbers were counted as one lesion.

The collected data were computerized and statistically analyzed using Statistical Package for Social Science (SPSS) program version 25.0. Quantitative data were expressed as median and range. Qualitative data were represented as frequencies and relative percentages. Chi square test was used to calculate difference between qualitative variables. Cohen's kappa test was used to estimate the agreement between different methods of diagnosis. Validity data were calculated using Sensitivity, Specificity, Positive predictive value, negative predictive value and accuracy. P value of < 0.05 indicates significant results and P value of < 0.001 indicates highly significant results.

Results

This retrospective cohort study enrolled 43 patients with female predominance 34 (79%) and 9 males (21%) with median age 55 years and range 34–59 years. Regarding the histopathological analysis, papillary type represented 33(76.7%) out of 43 patients, while follicular type was less than 10 (23.3%). According to the American Joint Cancer Committee (AJCC) TNM staging system 8th edition, the majority of the patients (76.7%) were at stage IV, while the remainder of the patients were represented almost equally at stages I, II, III (Table 1).

Table 1 Clinico-pathological data of the studied group
Full size table

Two patients out of 43, in whom diagnostic 131I WBS and US revealed only small recurrence in thyroid bed with significantly high serum Tg.18FDG PET/CT was done which revealed 3 cervical LN metastases, the dimensions of the smallest LN were 1.1 × 0.8 cm. Those patients were referred to surgery before receiving 131I therapy so they were excluded from the comparison between 18FDG PET/CT and 131I Tx WBS.

Performance of 18 FDG-PET/CT

The 18FDG-PET/CT detected tumor recurrent lesions in 35 (81.3%) patients with statistically significant relation between positivity of 18FDG-PET/CT and old age, female sex, high tumor stage and progressive course as 94.5% of patients equal or older than 55 years, 91.1% of females,75 and 97% of patients in stage III and IV and 97%showed progressive course. compared to 0% of patients with positive 18FDG-PET/CT < 55 years old, 44.4% of males, 0% of patients in stage I and II and 30% with regressive course (P value = 0.000, 0.001, < 0.001 and 0.000, respectively) (Table 2).

Table 2 Relation between positivity of 18FDG-PET/CT and age, sex, DTC staging and outcome
Full size table

Comparison between 18 FDG-PET/CT and 131 I TxWBS

In one patient 131ITxWBS falsely revealed skull osseous deposit that was attributed to surgical intervention and also 18FDG-PET/CT falsely reported cervical LN metastasis (1 lesion) in one patient, which was confirmed to be sarcoidosis by FNA biopsy.

Based on lesion analysis (Table 3) 18FDG-PET/CT could detect more lesions compared to 131ITxWBS [98 (79%), 87 (70.2%) out of 124] lesions, respectively. Regarding the different organs, PET/CT detected 52 out of 61 (85.2%) versus 48(78.6%) detected by TxWBS. Kappa value of agreement was poor between each technique and the confirmatory different tools; however, statistically significant good agreement between 18FDG-PET/CT and 131I TxWBS was noted (Kappa 0.78 and p < 0.001) (Table 3).

Table 3 Organ- and lesion-based analysis by 18FDG-PET/CT and 131I TxWBS in the context of histopathology, conventional radiological tools and lesion behavior over time
Full size table

18FDG-PET/CT could detect additive lesions compared to 131I TxWBS in 18 patients, while 131I TxWBS could detect additive lesions in only 6 patients.

18FDG-PET/CT has higher sensitivity than that of 131ITxWBS either based on lesion or organ analysis (78.2% vs. 69.4 and 85.2% vs. 77%, respectively) (Tables 4, 5).

Table 4 Diagnostic performance of 18FDG-PET/CT and 131I WBS based on lesion analysis in relation to histopathological results, conventional radiological tools and lesion behavior overtime
Full size table
Table 5 Diagnostic performance of 18FDG-PET/CT and 131IWBS based on organ analysis in relation to histopathological results, conventional radiological tools and lesion behavior overtime
Full size table

Impact of 18 FDG-PET/CT on the treatment plan

Twenty-five patients (58.2%) out of the 43 patients revealed no change in management (8 patients with negative 18FDG-PET/CT and 17 with positive 18FDG-PET/CT), while 18FDG-PET/CT could change the treatment plan in 18 (41.8%) patients out of 43; in two patients, WBS and US revealed only small recurrence in thyroid bed with significantly high serum Tg, so 18FDG PET/CT was done which revealed cervical lymph nodes (LN) metastases; therefore, the treatment plan was changed from only RAI therapy to pre-RAI therapy neck dissection (Fig. 1). Besides, 18FDG-PET/CT detected symptomatic osseous deposits that were missed by diagnostic and post-therapeutic WBS in seven patients that necessitated external radiation after receiving 131I therapeutic dose instead of only radioactive iodine (RAI) (Fig. 2). Also large hepatic metastasis was detected by18FDG-PET/CT in one patient with maximum standard uptake value (SUVmax) 30 in addition to recurrence in thyroid bed, while the diagnostic 131I WBS and post-therapeutic scans revealed only recurrence in thyroid bed, the decision was taken to undergo surgical excision of the hepatic metastasis then patient will receive RAI dose. Unfortunately, the surgery was postponed as the patient was surgically unfit, so he received his 131I therapeutic dose only. Moreover, adjustment of the RAI dose from 5.55 GBq (150 mCi) to 7.4 GBq (200 mCi) in six patients in consideration with their lung and bone recurrences determined by 18FDG-PET/CT, which were not detected by the conventional radiological tools. In two patients 18FDG-PET/CT demonstrated thyroid recurrence in operative thyroid bed encroaching on larynx and tracheal lumen which warranted surgical referral before RAI; however, one patient refused the surgical approach and the other was unfit for surgery so both patients received their therapeutic 131I doses only. It was noticed that TxWBS detected the lesions but unfortunately failed to characterize the lesion as accurately as 18FDG-PET/CT did (Table 6).

Fig. 1
figure 1

60 year old male patient with stage III papillary thyroid cancer who underwent total thyroidectomy then he received radioactive iodine ablative dose. During follow up he was represented by elevated level of I diagnostic WBS revealed only small sized recurrent thyroid 131 and ng/ml While both neck US 60, serum Tg-FDG18 was done for proper evaluation of the condition. (A1, A2); Axial FDG-PET/CT18, cancer. Therefore (arrows) sections reveal bilateral metastatic cervical LNs level II PET/CT (B) 131I diagnostic WBS shows only iodine avid residual thyroid tissue in the operative thyroid bed (arrow)

Full size image
Fig. 2
figure 2

Fifty-seven-year-old female patient with stage III differentiated follicular thyroid cancer underwent total thyroidectomy and 131I ablation. During follow-up, patient was represented by elevated serum Tg level; 200 ng/ml. Diagnostic WBS revealed only small recurrent thyroid tissue in thyroid operative bed (not available), so 18FDG-PET/CT was done to detect the possibility of hidden metastases. A 18FDG-PET/CT axial, sagittal and coronal sections reveal thyroid distant metastases; supraclavicular region LN, dorsal and lumbar vertebrae, paraspinal mass, pelvic bones and left femur (arrows) suggesting dedifferentiating nature of these lesions. B 131I-post-therapeutic WBS shows only bifocal iodine avid recurrent thyroid tissue at operative bed (arrow)

Full size image
Table 6 Impact of 18FDG-PET/CT on treatment management
Full size table

Discussion

Long years ago, 18FDG-PET/CT has been widely used as a tumor-seeking agent for various cancers. Nevertheless, researches on its role in thyroid cancer staging appeared only in the mid-1990s [31].

In recent years, it is obvious that 18FDG-PET/CT has a major role in thyroid cancer management but its utility in patients with recurrent DTC should be tailored according to circumstance of each patient [32].

In general, the role of 18FDG-PET/CT in initial staging and follow-up of low-risk patients with DTC is limited [33]. Conversely, in patients with more aggressive thyroid cancers, 18FDG-PET/CT is a very useful tool for determining the extent of metastatic disease [34, 35]. Also, for prognostic purposes and treatment response assessment [33, 36]. Moreover, Abraham et al. in their study stated that performing 18FDG-PET/CT in patients with recurrent/persistent DTC should take into account not only Tg levels or 131I WBS findings, but also, should be on the basis of clinical and histopathological features and their individual risk [33].

Schönberger et al. stated that, iodine-avid lesions of DTC usually have low or absent FDG uptake with a positive correlation between expression of glucose transporter 1 (GLUT1) and dedifferentiation of thyroid cancer cells [37]. Moreover, Piccardo et al. suggested the occurrence of iodine-concentrating metastases with high glucose uptake [31].

Some researchers declared that 18FDG-PET/CT has been shown to be a valuable diagnostic tool for the detection not only of 131I non-avid lesions, but also of 131I avid lesions of metastatic DTC [38].

Treglia et al. in a review article done in 2013 stated that; 18FDG-PET/CT and 131I WBS may provide complementary information useful in the restaging of DTC patients [38]. Moreover, Piccardo et al. believe that 18FDG-PET/CT may change the therapeutic approach in a stage-IV DTC subgroup of patients [31].

In the current study; 18FDG-PET/CT detected lesions in 35 (81.3%) out of 43 patients which goes with that declared by Loboulleux et al. in their study that enrolled 47 patients with DTC after thyroidectomy and 131I treatment, 18FDG-PET/CT was done for only 34 patients. The percentage of positive 18FDG-PET/CT among those with positive Tx 131I WBS was 5 out of 6 patients (83.3%) and also concordant with Piccardo et al. in their study which enrolled 20 stage-IV DTC patients with elevated Tg levels associated with positive I31I WBS. The 18FDG PET/CT was positive in 16 out of 20 patients (80%). On the other hand, the rate of 18FDG-PET/CT lesion detection in the current study is lower than that of Liu et al. and higher than that of Sandra et al. and Oh et al. studies. Liu et al. study enrolled 212 DTC patients, among 59 patients with positive TxWBS the 18FDG-PET/CT positivity was 51(86.4%). On the other hand, Sandra et al. in their study which enrolled 90 patients with DTC after first 131 I ablation 18FDG-PET/CT was positive in 13(40%) out of 32 patients with positive I131 Tx WBS. Regarding Oh et al. study which enrolled 140 only 30 patients of the total number were positive in WBS and only 16 (53.3%) of them were positive in 18FDG-PET/CT [2, 24, 39,40,41]. this variation may be attributed to difference in population in each study.

The sensitivity of 18FDG-PET/CT based on lesion analysis in our study more or less goes with that has been detected by Piccardo et al. (78.2% vs. 80%) meanwhile, obviously lower than that stated by Riemann et al. (91%) among positive131 I WBS subgroup. These differences may be attributed to the differences in study population regarding the risk stratification [31, 39, 42].

Obviously, the specificity of 18FDG-PET/CT in our study was significantly lower than that was calculated by Riemann et al. in their study (50% vs. 89%). We believe that small sample size did not enable precise assessment of the specificity [42].

In the current study, the sensitivity of 131I TxWBS based on lesions analysis goes with that measured by Piccardo et al. in their study (69.4% vs. 67%). Reduction in sensitivity may be attributed to an increased number of patients in III and IV stages on expense of I and II stages.

In our study 18FDG-PET/CT findings led to modifications in the management of 41.6% which was less than that declared by Piccardo et al. in their study 55%, this may be explained by decrease percentage of patients in stage IV compared with that in Piccardo et al. 76.7% versus 100%, respectively [31].

Our result was higher that detected by Maamoun et al. in their study which enrolled 126 patients who underwent 18F FDG PET/CT initially before 131I ablation 30.6% [43].

Limitation

One of the limitations of the study was non-availability of histopathological examination in a number of patients to confirm recurrences for both practical and ethical reasons. We admit that small sample size influenced proper assessment of specificity and also fair comparison between low and high risk groups, which may be taken in consideration in future studies. Also another limitation is comparing 18FDG-PET/CT with planer 131 I WBS and not with single photon emission tomography/computerized tomography (SPECT/CT).

Conclusion

18FDG-PET/CT may be complementary to 131ITxWBS in high-risk DTC with impact on treatment strategy (Additional files 1, 2, 3: Fig. 1).

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

18FDG PET/CT:

18F-fluorodeoxyglucose-positron emission tomography/computerized tomography

DTC:

Differentiated thyroid cancer patients

TxWBS:

Post-therapeutic whole body scan

PTC:

Papillary thyroid carcinoma

FTC:

Follicular thyroid carcinoma

LN:

Lymph node

FNA:

Fine needle aspiration

US:

Ultrasound

Tc99mMDP:

Technetium methylene diphosphonate

Tg:

Thyroglobulin

TSH:

Thyroid stimulating hormone

GE:

General electric

SPSS:

Statistical Package for Social Science

AJCC:

American Joint Cancer Committee

SUVmax:

Maximum standard uptake value

GLUT1:

Glucose transporter 1

RAI:

Radioactive iodine

SPECT/CT:

Single photon emission computed tomography/computed tomography

References

  1. Luo X, Wu ACYZYJBZJ (2019) Analysis of risk factors for postoperative recurrence of thyroid cancer. JBUON 24(2):813–818

    PubMed  Google Scholar 

  2. Naoum GE, Morkos M, Kim B, Arafat W (2018) Novel targeted therapies and immunotherapy for advanced thyroid cancers. Mol Cancer 17(1):51. https://doi.org/10.1186/s12943-018-0786-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kim J, Gosnell JE, Roman SA (2020) Geographic influences in the global rise of thyroid cancer. Nat Rev Endocrinol 16(1):17–29. https://doi.org/10.1038/s41574-019-0263-x3

    Article  PubMed  Google Scholar 

  4. Vaccarella S, Franceschi S, Bray F, Wild CP, Plummer M, Dal Maso L (2016) Worldwide thyroid-cancer epidemic? The increasing impact of over diagnosis. N Engl J Med 375(7):614–617. https://doi.org/10.1056/NEJMp1604412

    Article  PubMed  Google Scholar 

  5. Davies L, Welch HG (2014) Current thyroid trends in the United States. JAMA Otolaryngol Head Neck Surg 140(4):317–322. https://doi.org/10.1001/jamaoto.2014.1

    Article  PubMed  Google Scholar 

  6. Davies L, Welch HG (2006) Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA 295(18):2164–2167. https://doi.org/10.1001/jama.295.18.2164

    Article  CAS  PubMed  Google Scholar 

  7. Davies L, Ouellette M, Hunter M, Welch HG (2010) The increasing incidence of small thyroid cancers: where are the cases coming from? Laryngoscope 120(12):2446–2451. https://doi.org/10.1002/lary.21076

    Article  PubMed  Google Scholar 

  8. Morris LG, Myssiorek D (2010) Improved detection does not fully explain the rising incidence of well-differentiated thyroid cancer: a population-based analysis. Am J Surg 200(4):454–461. https://doi.org/10.1016/j.amjsurg.2009.11.008

    Article  PubMed  PubMed Central  Google Scholar 

  9. Chen L, Luo Q, Shen Y, Yu Y, Yuan Z, Lu H et al (2008) Incremental value of 131I SPECT/CT in the management of patients with differentiated thyroid carcinoma. JNM 49(12):1952–1957. https://doi.org/10.2967/jnumed.108.052399

    Article  PubMed  Google Scholar 

  10. Moustafa H, Taalab K (2012) Role of 18F-FDG-PET/CT in patients with differentiated thyroid cancer who present with elevated thyroglobulin and negative 131I whole body scan. EJNM 5(5):39–46. https://doi.org/10.21608/EGYJNM.2012.5481

    Article  Google Scholar 

  11. Yang x, Liang j, Li TJ, Yang K, Liang D, Yu Z, et al (2015) Postoperative stimulated thyroglobulin level and recurrence risk stratification in differentiated thyroid cancer. Chin Med J (Engl) 128(8):1058–1064. https://doi.org/10.4103/0366-6999.155086

    Article  CAS  Google Scholar 

  12. Schlumberger MJ (1998) Papillary and follicular thyroid carcinoma. N Engl J Med 338(5):297–306. https://doi.org/10.1056/NEJM199801293380506

    Article  CAS  PubMed  Google Scholar 

  13. Hay ID, Bergstralh EJ, Goellner JR, Ebersold JR, Grant CS (1993) Predicting outcome in papillary thyroid carcinoma: development of a reliable prognostic scoring system in a cohort of 1779 patients surgically treated at one institution during 1940 through 1989. Surgery 114(6):1050–1057 (discussion 1057-8)

    CAS  PubMed  Google Scholar 

  14. Lin JD, Huang MJ, Juang JH, Chao TC, Huang BY, Chen KW et al (1999) Factors related to the survival of papillary and follicular thyroid carcinoma patients with distant metastases. Thyroid 9(12):1227–1235. https://doi.org/10.1089/thy.1999.9.1227

    Article  CAS  PubMed  Google Scholar 

  15. Wartofsky L, Sherman SI, Gopal J, Schlumberger M, Hay ID (1998) The use of radioactive iodine in patients with papillary and follicular thyroid cancer. J Clin Endocrinol Metab 83(12):4195–4203. https://doi.org/10.1210/jcem.83.12.5293-1

    Article  CAS  PubMed  Google Scholar 

  16. Schlumberger MJ (1999) Diagnostic follow-up of well-differentiated thyroid carcinoma: historical perspective and current status. J Endocrinol Invest 22(11):3–7

    CAS  PubMed  Google Scholar 

  17. Giannoula E, Iakovou I, Verburg FA (2018) Long term quality of life in differentiated thyroid cancer patients after thyroidectomy and high doses of 131I with or without suppressive treatment. Hell J Nucl Med 21(1):69–73. https://doi.org/10.1967/s002449910708

    Article  PubMed  Google Scholar 

  18. Ronga G, Toteda M, D’Apollo R, De Cristofaro F, Filesi M, Acqualagna G et al (2012) Lymph node metastases from differentiated thyroid carcinoma: does radioiodine still play a role? Clin Ter 163:377–381

    CAS  PubMed  Google Scholar 

  19. Choudhury PS, Gupta M (2018) Differentiated thyroid cancer theranostics: radioiodine and beyond. Br J Radiol 91(1091):20180136. https://doi.org/10.1259/bjr.20180136

    Article  PubMed  PubMed Central  Google Scholar 

  20. Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE et al (2016) 2015 American Thyroid association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: the American Thyroid Association guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid 26:1–133. https://doi.org/10.1089/thy.2015.0020

    Article  PubMed  PubMed Central  Google Scholar 

  21. Miller ME, Chen Q, Elashoff D, Abemayor E, St John M (2011) Positron emission tomography and positron emission tomography-CT evaluation for recurrent papillary thyroid carcinoma: meta-analysis and literature review. Head Neck 33(4):562–565. https://doi.org/10.1002/hed.21492

    Article  PubMed  Google Scholar 

  22. Makeieff M, Burcia V, Raingeard I, Eberlé MC, Cartier C, Garrel R et al (2012) Positron emission tomography-computed tomography evaluation for recurrent differentiated thyroid carcinoma. Eur Ann Otorhinolaryngol Head Neck Dis 129(5):251–256. https://doi.org/10.1016/j.anorl.2012.01.003

    Article  CAS  PubMed  Google Scholar 

  23. Feine U, Lietzenmayer R, Hanke JP, Held J, Wöhrle H, Müller-Schauenburg W (1996) Fluorine-18-FDG and iodine-131-iodide uptake in thyroid cancer. JNM 37(9):1468–1472

    CAS  PubMed  Google Scholar 

  24. Leboulleux S, El Bez I, Borget I, Elleuch M, Déandreis D, Al Ghuzlan A et al (2012) Postradioiodine treatment whole-body scan in the era of 18-fluorodeoxyglucose positron mission tomography for differentiated thyroid carcinoma with elevated serum thyroglobulin levels. Thyroid 22(8):832–838. https://doi.org/10.1089/thy.2012.0081

    Article  CAS  PubMed  Google Scholar 

  25. Dietlein M, Scheidhauer K, Voth E, Theissen P, Schicha H (1997) Fluorine-18 fluoro-deoxyglucose positron emission tomography and iodine-131 whole-body scintigraphy in the follow-up of differentiated thyroid cancer. Eur J Nucl Med 24(11):1342–1348. https://doi.org/10.1007/s002590050158

    Article  CAS  PubMed  Google Scholar 

  26. Dionigi G, Fama’ F, Pignata SA, Pino A, Pontin A, Caruso E et al (2020) Usefulness of PET-CT scan in recurrent thyroid cancer. World J Otorhinolaryngol Head Neck Surg 6(3):182–187. https://doi.org/10.1016/j.wjorl.2020.02.008

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kolodziej M, Saracyn M, Lubas A, Brodowska-Kania D, Mazurek A, Dziuk M et al (2021) Evaluation of the usefulness of positron emission tomography with [18F]fluorodeoxylglucose performed to detect non-radioiodine avid recurrence and/or metastasis of differentiated thyroid cancer: a preliminary study. Nucl Med Rev 24(2):63–69. https://doi.org/10.5603/NMR.2021.0017

    Article  Google Scholar 

  28. Almeida LS, Araújo ML, Santos AO, Montali da Assumpção LV, Lima ML, Ramos CD et al (2020) Head-to-head comparison of F-18 FDG PET/CT in radioidine refractory thyroid cancer patients with elevated versus suppressed TSH levels a pilot study. Heliyon 6(3):e03450. https://doi.org/10.1016/j.heliyon.2020.e03450

    Article  PubMed  PubMed Central  Google Scholar 

  29. Klain M, Nappi C, Nicolai E, Romeo V, Piscopo L, Giordano A et al (2000) Comparison of simultaneous (18) F-2-[18F] FDG PET/MR and PET/CT in the follow-up of patients with differentiated thyroid cancer. Eur J Nucl Med Mol Imaging 47(13):3066–3073. https://doi.org/10.1007/s00259-020-04938-0

    Article  CAS  Google Scholar 

  30. Li H, Chen X, Zhang Y, Wang K, Gao Z (2021) Value of 18F-FDG hybrid PET/MR in differentiated thyroid cancer patients with negative 131I whole-body scan and elevated thyroglobulin levels. Cancer Manag Res 13:2869–2876. https://doi.org/10.2147/CMAR.S293005

    Article  PubMed  PubMed Central  Google Scholar 

  31. Piccardo A, Foppiani L, Morbelli S, Bianchi P, Barbera F, Biscaldi E et al (2011) Could 18FDG-PET/CT change the therapeutic management of stage IV thyroid cancer with positive 131I whole body scan? Q J Nucl Med Mol Imaging 55(1):57–65

    CAS  PubMed  Google Scholar 

  32. Abraham T, Schöder H (2011) Thyroid cancer–indications and opportunities for positron emission tomography/computed tomography imaging. Semin Nucl Med 41(2):121–138. https://doi.org/10.1053/j.semnuclmed.2010.10.006

    Article  PubMed  Google Scholar 

  33. Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ et al (2009) Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 19(11):1167–1214. https://doi.org/10.1089/thy.2009.0110

    Article  PubMed  Google Scholar 

  34. Grabellus F, Nagarajah J, Bockisch A, Schmid KW, Sheu SY (2012) Glucose transporter 1 expression, tumor proliferation, and iodine/glucose uptake in thyroid cancer with emphasis on poorly differentiated thyroid carcinoma. Clin Nucl Med 37(2):121–127. https://doi.org/10.1097/RLU.0b013e3182393599

    Article  PubMed  Google Scholar 

  35. Treglia G, Annunziata S, Muoio B, Salvatori M, Ceriani L, Giovanella L (2013) The role of fluorine-18-fluorodeoxyglucose positron emission tomography in aggressive histological subtypes of thyroid cancer: an overview. Int J Endocrinol 2013:856189. https://doi.org/10.1155/2013/856189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Poisson T, Deandreis D, Leboulleux S, Bidault F, Bonniaud G, Baillot S et al (2010) 18F-fluorodeoxyglucose positron emission tomography and computed tomography in anaplastic thyroid cancer. Eur J Nucl Med Mol Imaging 37(12):2277–2285. https://doi.org/10.1007/s00259-010-1570-6

    Article  PubMed  Google Scholar 

  37. Schönberger J, Rüschoff J, Grimm D, Marienhagen J, Rümmele P, Meyringer R et al (2002) Glucose transporter 1 gene expression is related to thyroid neoplasms with an unfavorable prognosis: an immunohistochemical study. Thyroid 12(9):747–754. https://doi.org/10.1089/105072502760339307

    Article  PubMed  Google Scholar 

  38. Treglia G, Bertagna F, Piccardo A, Giovanella L (2013) 131I whole-body scan or 18FDG PET/CT for patients with elevated thyroglobulin and negative ultrasound? Clin Transl Imaging 1(3):175–183. https://doi.org/10.1007/s40336-013-0024-0

    Article  Google Scholar 

  39. Liu M, Cheng L, Jin Y, Ruan M, Sheng S, Chen L (2018) Predicting 131 I-avidity of metastases from differentiated thyroid cancer using 18FDG-PET/CT in postoperative patients with elevated thyroglobulin. Sci Rep 8(1):4352. https://doi.org/10.1038/s41598-018-22656-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Rosenbaum-Krumme SJ, Görges R, Bockisch A, Binse I (2012) 18F-FDG PET/CT changes therapy management in high-risk DTC after first radioiodine therapy. Eur J Nucl Med Mol Imaging 39:1373–1380. https://doi.org/10.1007/s00259-012-2065-4

    Article  PubMed  Google Scholar 

  41. Oh JR, Byun BH, Hong SP, Chong A, Kim J, Yoo SW et al (2011) Comparison of 131I whole-body imaging, 131I SPECT/CT, and 18FDG-PET/CT in the detection of metastatic thyroid cancer. Eur J Nucl Med Mol Imaging 38(8):1459–1468. https://doi.org/10.1007/s00259-011-1809-x

    Article  PubMed  Google Scholar 

  42. Riemann B, Uhrhan K, Dietlein M, Schmidt D, Kuwert T, Dorn R et al (2013) Diagnostic value and therapeutic impact of 18FDG-PET/CT in differentiated thyroid cancer. Nuklearmedizin 52(1):1–6. https://doi.org/10.3413/nukmed-0489-12-03

    Article  CAS  PubMed  Google Scholar 

  43. Maamoun N, Moustafa H, Zaher A, Fathy H (2020) Value of initial 18FDG-PET/CT in change of management of patients with differentiated thyroid cancer as compared to post ablative whole body iodine scan. Egypt J Nucl Med 21(2):34–49. https://doi.org/10.21608/EGYJNM.2020.140414

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Dina Elrefay, Department of public health and community medicine in Zagazig University for her helpful cooperation.

Funding

No funding was received for this research.

Author information

Authors and Affiliations

  1. Clinical Oncology and Nuclear Medicine Department, Zagazig University, Zagazig, Egypt

    Heba M. Abdelhamed, Amira E. Mohammed & Mona S. Fattahalla

  2. Nuclear Medicine Department, Assiut University, Asyut, Egypt

    HebatAllah Askar

Authors
  1. Heba M. Abdelhamed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amira E. Mohammed
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mona S. Fattahalla
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. HebatAllah Askar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors have read and approved the manuscript. Study concept and design were proposed by HMA and HAA. HMA, AEM and MSF were responsible for patients' recruitment, follow-up and acquisition of data. Procedures were done by HMA, AEM and MSF. Analysis and interpretation of data and drafting of the manuscript were done by HMA and HAA. Revision of the manuscript was done by HMA and HAA. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Heba M. Abdelhamed.

Ethics declarations

Ethics approval and consent to participate

The study design was approved by institutional review board of clinical oncology and nuclear medicine department in Zagazig University in accordance with the 1964 Helsinki declaration. Number of approval: 6382. Informed written consent was waived because the study was retrospective.

Consent for publication

The patients' consent to publish the data contained within this study was waived because of the retrospective design of the study.

Competing interests

All authors declared that they had no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1.

Axial 18FDG-PET/CT section reveals metastatic cervical LNs level II bilaterally more prominent on the left side (arrows).

Additional file 2.

Axial 18FDG-PET/CT section reveals bilateral metastatic cervical LNs level II (arrows).

Additional file 3.

131I diagnostic WBS shows only iodine avid residual thyroid tissue in the operative thyroid bed (arrow).

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdelhamed, H.M., Mohammed, A.E., Fattahalla, M.S. et al. Additive value of 18FDG-PET/CT to positive 131I whole body scan in recurrent differentiated thyroid cancer patients with potential influence on treatment strategy: single Egyptian center experience. Egypt J Radiol Nucl Med 53, 30 (2022). https://doi.org/10.1186/s43055-021-00692-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s43055-021-00692-x

Keywords