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Unit of Endocrinology, Scientific Institute Casa Sollievo della Sofferenza (M.T., U.C.), 71013 S. Giovanni Rotondo, Foggia, Italy; Cervello Hospital (M.A., G.D’A.), 90100 Palermo, Italy; Tinchi-Pisticci Hospital (R.B.), 75020 Matera, Italy; Bentivoglio Hospital (D.M.), 40010 Bologna, Italy; Department of Biomedical Sciences, University of Catania (S.T.), 95100 Catania, Italy; Department of Experimental and Clinical Medicine, University Magna Graecia (G.C., R.S., F.A.), 88100 Catanzaro, Italy; and Department of Experimental Medicine and Pathology (E.F.) and Clinical Sciences (S.F.), University La Sapienza, 00161 Rome, Italy
Address all correspondence and requests for reprints to: Dr. Sebastiano Filetti, 2a Clinica Medica, Dipartimento di Scienze Cliniche, Universita’ degli Studi di Roma, La Sapienza, v.le del Policlinico, 155, 00161 Rome, Italy. E-mail:sebastiano.filetti{at}uniroma1.it.
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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80–85%) are classified as low risk for death, although some of them are at high risk for recurrence, including younger (<16 yr) or older (>45 yr) subjects, those with more aggressive histological subtypes, those with larger or infiltrating tumors, and those with initial lymph node metastases (1). In the past, a whole body scan with radioiodine (WBS) was considered the main tool for detecting persistent or recurrent disease during follow-up. Recent studies have demonstrated that thyroglobulin (Tg) determination is more sensitive, and diagnostic WBS is useless in the majority of these patients (8, 9, 10, 11, 12). Furthermore, the sensitivity of Tg measurement increases after TSH stimulation, either after thyroid hormone withdrawal (THW) or after administration of recombinant human TSH. Therefore, serum Tg determination is currently considered the gold standard in suspecting recurrences; however, 1) it does not allow localization of the recurrences (3, 4, 5, 13, 14); and 2) it is undetectable in 20% of patients with isolated lymph node metastases during T4 treatment and in 5% after THW (1). Finally, one important goal of follow-up is the early discovery of persistent or recurrent disease.
In the majority of PTC patients, persistent or recurrent disease is located in the neck, but the effective role of neck ultrasound examination (US) in its detection has not yet been well established; recently, some researchers have suggested its routine use, because it also seems able to detect loco-regional disease in some patients with undetectable stimulated serum Tg levels (7, 12, 15).
Our study focused on determining the sensitivity of neck US to detect lymph node metastases in a large cohort of low risk PTC patients during follow-up, carried out together with Tg determination and WBS, both performed after THW; another goal of the study was to determine whether US can provide an early discovery of persistent or recurrent disease compared with the other modalities.
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Subjects and Methods |
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Four hundred ninety-three consecutive low risk PTC patients were operated on between October 1994 and December 1997 in five institutions. Subjects were considered at low risk for death according to the following criteria: age more than 16 yr and less than 45 yr, thyroid tumor with a diameter less than 1.5 cm and with no invasion of the thyroid capsule, and absence of distant metastases (16).
All patients were treated with near-total thyroidectomy and lymph node dissection. Forty-four subjects were not treated with radioiodine because of a glandular residue less than 2 ml at US examination, indicating the completeness of total thyroidectomy. Instead, 449 patients were treated postoperatively with radioiodine (dose, 1.1–2.6 GBq) for ablation of significant thyroid remnant; in 412 cases a WBS performed 4–7 d after the ablative dose did not disclose 131I uptake foci outside the thyroid bed. In the 37 patients with foci of uptake outside the thyroid bed, additional surgery and/or 131I treatment were performed. These latter patients were not included in the study because they had known persistent disease (only patients with no evidence of disease were included) (8, 12). In addition, patients with interferences in the Tg assay (recovery test <70% or presence of anti-Tg antibodies) were previously excluded from the study (n = 56). Overall, data on the follow-up of a homogeneous series of 456 consecutive patients (374 women and 82 men) who had radical surgery and no clinical signs of residual disease (i.e. patients at low risk for recurrence) were considered (mean age, 31 ± 11 yr; range, 17–45 yr). By definition, all 456 patients were classified as T1, M0; 381 were classified as N0, 69 as N1, and six as Nx (16) (Table 1
). L-T4 treatment was initiated after surgery or radioiodine ablation with the aim of obtaining a TSH level less than 0.5 µU/ml (17). At 3 months, TSH and free T3 levels were determined. All 456 patients had a first follow-up evaluation 12 months after radioiodine ablation or surgery (if not treated by radioiodine). All subjects had further follow-up examinations, with the same modalities, at least 2–3 and 4.5–5.5 yr after the initial treatment. Five patients dropped out at the last follow-up.
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The procedures followed were in accordance with the Helsinki Declaration of 1975, as revised in 1983. The follow-up examination consisted of a neck US examination and a WBS with serum Tg measurement after THW (TSH, >30 µU/ml). Patients were placed on a low iodine diet and instructed to avoid iodine-containing foods for at least 20 d before the study. A dose of 74–185 MBq radioiodine was given, and scanning was performed 2 d later.
Based on THW-Tg levels, patients were classified as Tg negative [Tg(–); 
1 ng/ml] or Tg-positive [Tg(+); >1 ng/ml]. Tg levels of 10 ng/ml or more were considered suspicious for persistent disease (8), but over the years considered in the study, additional 131I treatment, even in the absence of any other evidence of disease, was warranted only in those with higher serum Tg levels (>25 ng/ml). Lymph nodes were considered suspicious by one of the following US features: diameter of 4 mm or more, rounded shape, and/or presence of microcalcifications and/or cystic component. Adjunctive characteristics of suspected malignancy were absence of hyperechoic hilus and/or hypervascularization at color Doppler examination (7, 12, 18). To confirm recurrence in US-suspected neck lymph nodes, a US-guided fine needle aspiration biopsy (FNAB) was performed for cytology as well, especially for very small nodes (<8 mm), for genetic analysis of fluid aspirate (i.e. by assessing TSH receptor and thyroglobulin mRNA levels) (19, 20). In case of positivity, further surgery was performed. When FNAB was not adequate for diagnosis, an additional FNAB was performed 6–12 months later.
Methods
Serum Tg was measured by immunoradiometric assay (Byk-Sangtec, Dietzenbach, Germany; or Brahms, Berlin, Germany), with a clinical sensitivity of 1 ng/ml (1, 2, 8, 11, 12, 13). Tg recovery was evaluated in the same assay after the addition of 10 µl of the spiking solution containing 50 ng/ml (normal recovery values, 70–130%). Serum TSH and anti-Tg antibody titers were measured by commercial kits.
131I-WBS was performed using either a double 
-camera equipped with high energy collimators and thick crystals or a rectilinear scanner (scan speed, 5 cm/min); a total count of at least 140,000 cpm was recorded. Neck uptake in the median region could be located to the thyroid bed with the use of anatomical marks, and the location was further confirmed by neck US, which showed no abnormality in lymph node areas. In all of these cases uptake was less than 0.5%, and WBS was considered negative (12). Accordingly, WBS is presented as positive in Results only in cases of pathological uptake (outside the thyroid bed).
Neck US was performed using color Doppler scanners equipped with multifrequency probes (7.5–12 MHz). Thyroid remnants and lymph node metastases volumes were calculated as the product of antero-posterior x transverse x longitudinal diameters x 0.52 (ellipsoid formula) (21).
Statistical analysis
Data are expressed as the mean ± SD. Differences between proportions were evaluated using 
2 or Fisher’s exact test when appropriate. The correlation between serum Tg levels and the diameter of lymph node metastases was tested using a nonparametric method (Spearman). The sensitivity, specificity, and global accuracy of WBS, US plus FNAB, and THW-Tg determination vs. histological examination were assessed. The positive predictive values (PPVs) of serum THW-Tg levels between 1 and 10 ng/ml and greater than 10 ng/ml and the negative predictive value of the combination of negative serum THW-Tg levels and negative neck US examination during follow-up were also determined.
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Results |
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Overall, 38 (8.3%) patients with lymph node metastases were identified by neck US examination plus FNAB. The clinical characteristics and the diagnostic procedures followed to establish persistent or recurrent disease are illustrated in Table 2. However, no significant difference in the prevalence of metastases between previously radioiodine-treated and nontreated patients was found.
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Frequency of disease persistence or recurrence during follow-up (Table 3)
First year follow-up. Overall, 335 of 456 patients (74%), after thyroid hormone withdrawal, were Tg(–) and 121 (26%) were Tg(+), 16 of them exhibiting undetectable serum Tg levels during T4 therapy that became detectable after THW (mean, 8 ± 7 ng/ml; range, 2–18). At this time, neck US showed suspicious lymph node metastases in 26 patients. FNAB and histology confirmed cervical node metastases in 21 of them [5 Tg(–) and 16 Tg(+) patients]. Conversely, WBS was positive in only five patients [all US and Tg(+)], showing in all cases uptake corresponding to pathological lymph nodes. Furthermore, node metastases were confirmed at subsequent follow-up in the other five US-positive [US(+)] patients [three Tg(–) and two Tg(+)]. Moreover, 12 US-negative patients with THW-Tg levels greater than 25 ng/ml were treated with 3.7 GBq 131I, and in no case was uptake outside the thyroid bed found.
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At 4.5–5.5 yr of follow-up, US showed suspicious nodes in six patients, and lymph node metastases were confirmed by FNAB and histology in five of them [one Tg(–) and four Tg(+)], including the two of them who were also WBS positive. At the end of follow-up only 14 patients (all previously radioiodine-treated) displayed detectable serum Tg levels (<10 ng/ml); to date, no evidence of persistent or recurrent disease has been detected in any of them (range of follow-up, 6–9 yr).
Positive and negative predictive values (Table 4)
During follow-up eight patients showed an increasing THW-Tg level [four Tg(–) and four Tg(+)]; in all cases, neck lymph node metastases were demonstrated. Consequently, the PPV of an increasing THW-Tg level was 100%. Conversely, 65 of 96 patients (67.7%) who displayed low positive serum THW-Tg levels (>1–10 ng/ml) at first follow-up became Tg(–) without any adjunctive treatment in the following 2 yr; no difference in the prevalence between previously radioiodine-treated or untreated patients was found.
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Diagnostic accuracy (Table 5)
The sensitivity of WBS vs. histology was 34.2%, the specificity was 100%, and the global accuracy was 94.5%. WBS discovered lymph node metastases in a total of 13 patients at the end of follow-up [all Tg(+)]. Consequently, all Tg(–) subjects had negative WBS.
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Finally, the sensitivity, specificity and global accuracy of US plus FNAB were 100% in all cases; they identified all 38 patients with lymph node metastases [31 Tg(+), including all WBS positive, and seven Tg(–) patients]. The difference between US plus FNAB and WBS sensitivities was statistically significant (2 = 12; P < 0.0005 vs. WBS).
Concordance between US and FNAB during follow-up ranged from 75–83%. In addition, all five patients that at first year follow-up showed suspected lymph nodes on US and negative FNAB [three Tg(–) and two Tg(+)], became FNAB positive in the following 1–2 yr; they underwent surgery, and pathological examination confirmed malignant lesions. This discrepancy in the time of detection of malignant node lesions among serum Tg determination, WBS, US, and FNAB is also shown in Table 6 for five patients who delayed surgery for various reasons. The positivity of US preceded that of WBS in all patients, preceded that of THW-Tg in four of five patients, and preceded that of FNAB in two of five patients.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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At first follow-up, performed 12 months after surgery or radioiodine administration, 335 patients (73.5%) were Tg(–); this high percentage is not surprising, because by definition all subjects were at low risk, being classified as stage I (16). Furthermore, about 68% of patients who were Tg(+) at first follow-up (either previously treated or not treated with radioiodine) with serum THW-Tg levels between 1 and 10 ng/ml became spontaneously Tg(–) in the following 2 yr. This finding confirms previously reported data reported by Pacini et al. (22) and Baudin et al. (23); the normalization of serum THW-Tg levels 2 or 3 yr after radioiodine treatment or surgery alone may be attributed to the delayed death of irradiated thyroid cells or the progressive atrophy of the small residual tissue, respectively. Consequently, it suggests that in these patients the finding of serum THW-Tg levels between 1 and 10 ng/ml at first follow-up (1 yr after the initial treatment) should not be considered definitely indicative of persistent or recurrent disease, because the majority of these subjects will show undetectable serum THW-Tg levels in the following 1 or 2 yr. In our opinion, this is a very important issue, because it can avoid many inappropriate radioiodine treatments. On the contrary, the finding of an increasing THW-Tg level during follow-up predicts persistent or recurrent disease (all eight patients in our series), confirming a recent report by Baudin et al. (23).
Diagnostic WBS was confirmed to be a low sensitivity tool in detecting recurrences (8, 9, 11, 12, 15). It was positive for cervical metastases in 13 Tg(+) patients. In contrast, neck US was able to individualize lymph node metastases in 38 patients (including all 13 WBS-positive subjects). Moreover, it is noteworthy that seven of 38 US(+) subjects were Tg(–); all but one (patient 1) had a single metastasis, and in all cases the diameter of the metastasis was less than 1 cm (Table 1
). Moreover, we were able to confirm a positive correlation between the volume of neck lymph node metastases and serum THW-Tg levels (24). This finding confirms the observation that small node metastases probably secrete quantities of Tg too small to be detectable in serum and strongly supports the usefulness of neck US in the first follow-up of all these patients [Tg(+) as well Tg(–)].
There is no doubt that better prognosis of PTC patients depends on primary treatment and appropriate follow-up. In low risk patients, relapses are mainly loco-regional and are usually detected within the first 4–5 yr after initial treatment; however, recurrent disease may appear throughout the patient’s life (1). Our study clearly demonstrates that US can easily detect local recurrences in Tg(–) patients also and presents useful information concerning surgical retreatment. Moreover, an important finding in our study is that US allows very early detection of suspected recurrences that can precede not only serum THW-Tg and WBS positivity, but also cytological confirmation (this latter finding is often due to the small size of the affected lymph nodes). In this regard, the utilization of genetic analysis greatly improves the ability to confirm the presence of metastatic tissue (19, 20). Indeed, the importance of discovering and operating on these often very small loco-regional lymph node metastases is actually unknown in terms of prognosis, because we cannot say whether such small lesions would have become clinically relevant in the future. At present, however, surgery should be considered.
Our final point is that the combination of serum negative THW-Tg and negative neck US examination, at least in the first 5 yr follow-up, clearly indicates a risk of local recurrence close to 0%; this confirms, in a larger series of patients, what was already reported for either Tg-negative or Tg-negative/US-negative subjects (8, 15). The present data confirm that two prognostic groups should be individualized according to findings at the first year control, and each of these groups should be submitted to a different protocol for subsequent follow-up regardless of the initial prognostic indicators.
In conclusion, our study demonstrates that in the follow-up of low risk PTC patients 1) residual or recurrent disease is infrequent (38 of 456, 8.3%); 2) neck lymph node metastases appear as the unique localization, and the majority of recurrences (>85%) occur within the first 3 yr after the initial treatment; 3) a THW-Tg level between 1 and 10 ng/ml at first follow-up has a low PPV for persistent or recurrent disease, because it will become undetectable in the majority of cases during the following 1 or 2 yr; 4) WBS is a low sensitivity tool and does not add any further information to US plus FNAB results; 5) serum Tg levels depend on sizes of the metastases, and US, but not WBS, is able to localize small neck lymph node metastases in some Tg(–) patients: indeed, US allows earlier detection of suspicious lymph nodes, preceding not only WBS, but sometimes also serum Tg and FNAB positivity; 6) the risk of local recurrences in US-negative/Tg(–) patients is negligible; 7) the finding of an increasing serum THW-Tg level has a PPV of 100% for persistent/recurrent disease. Our data suggest that neck sonography together with determination of serum Tg levels after TSH stimulation should be considered the imaging modality of choice for postoperative surveillance in these patients. Consequently, we suggest a first follow-up (1 yr after initial treatment) simply based upon clinical control, US assessment (in all patients, including those with normal neck palpation), and stimulated (after withdrawal or recombinant human TSH) serum Tg determination. At subsequent follow-ups, 1) US should not be mandatory at each examination in initial Tg(–) and US-negative subjects, but is strongly suggested in all the other cases; 2) Tg determination should be repeated 1 yr later after exogenous or endogenous TSH stimulation only in initial Tg(+) patients without any evidence of residual disease; and 3) Tg measurement during therapy could be sufficient in all other cases.
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Footnotes |
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Abbreviations: FNAB, Fine needle aspiration biopsy; (–), negative; (+), positive; PPV, positive predictive value; PTC, papillary thyroid carcinoma; Tg, thyroglobulin; THW, thyroid hormone withdrawal; US, ultrasonography; WBS, whole body scan.
Received September 9, 2003.
Accepted March 18, 2004.
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