Utility of solid area diameter in management of cystic papillary thyroid carcinoma

in Endocrine Connections
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Ayana Suzuki Department of Diagnostic Pathology and Cytology, Kuma Hospital, Kobe, Japan

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Mitsuyoshi Hirokawa Department of Diagnostic Pathology and Cytology, Kuma Hospital, Kobe, Japan

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Izumi Otsuka Secretary Section, Kuma Hospital, Kobe, Japan

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Akihiro Miya Department of Surgery, Kuma Hospital, Kobe, Japan

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Akira Miyauchi Department of Surgery, Kuma Hospital, Kobe, Japan

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Takashi Akamizu Department of Internal Medicine, Kuma Hospital, Kobe, Japan

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Correspondence should be addressed to A Suzuki: suzuki01@kuma-h.or.jp
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Papillary thyroid carcinoma (PTC) with marked cystic formation (CPTC) is not a subtype of PTC, and its clinical characteristics have not been fully investigated. This study aimed to clarify the clinical and pathological characteristics of CPTC and propose important indicators for its clinical management. Thirty-three CPTC nodules with cystic areas occupying >50% of their volume were examined. Two matched controls (MCs) were prepared, one with tumor diameter matched for whole tumor diameter (WTD) of CPTCs and the other with tumor diameter matched for solid area diameter (SAD) of CPTCs. The mean age of patients with CPTC was 55.2 years significantly older than that in SAD-MCs. Of the CPTCs, 69.7% were classified as highly suspicious by ultrasonography, and the prevalence was lower than that in WTD-MCs (88.9%) and SAD-MCs (91.5%). Total thyroidectomy was performed in 69.7% of CPTC cases, which was significantly less frequent than that in WDT-MCs (91.7%) and similar to that in SAD-MCs (76.1%). Histologically, CPTCs exhibited two characteristic findings: invasion from the solid area into the surrounding normal thyroid tissue and granulation tissue around the cystic wall. The frequencies of the cases with pathological lateral node metastasis, extrathyroidal extension, and Ki-67 labeling index ≥5% in CPTCs were significantly lower than those in WTD-MCs and relatively similar to those in SAD-MCs. In the surgical strategy and prognosis of CPTC, the evaluation of tumor size should be based on SAD rather than on WTD. We advocate measuring not only WTD but also SAD in CPTC.

Abstract

Papillary thyroid carcinoma (PTC) with marked cystic formation (CPTC) is not a subtype of PTC, and its clinical characteristics have not been fully investigated. This study aimed to clarify the clinical and pathological characteristics of CPTC and propose important indicators for its clinical management. Thirty-three CPTC nodules with cystic areas occupying >50% of their volume were examined. Two matched controls (MCs) were prepared, one with tumor diameter matched for whole tumor diameter (WTD) of CPTCs and the other with tumor diameter matched for solid area diameter (SAD) of CPTCs. The mean age of patients with CPTC was 55.2 years significantly older than that in SAD-MCs. Of the CPTCs, 69.7% were classified as highly suspicious by ultrasonography, and the prevalence was lower than that in WTD-MCs (88.9%) and SAD-MCs (91.5%). Total thyroidectomy was performed in 69.7% of CPTC cases, which was significantly less frequent than that in WDT-MCs (91.7%) and similar to that in SAD-MCs (76.1%). Histologically, CPTCs exhibited two characteristic findings: invasion from the solid area into the surrounding normal thyroid tissue and granulation tissue around the cystic wall. The frequencies of the cases with pathological lateral node metastasis, extrathyroidal extension, and Ki-67 labeling index ≥5% in CPTCs were significantly lower than those in WTD-MCs and relatively similar to those in SAD-MCs. In the surgical strategy and prognosis of CPTC, the evaluation of tumor size should be based on SAD rather than on WTD. We advocate measuring not only WTD but also SAD in CPTC.

Introduction

Papillary thyroid carcinoma (PTC) can be associated with the formation of cysts. PTCs with cystic components occupying more than 50% of the tumor account for 1.3–2.5% of all PTCs (1, 2). These tumors are known as cystic papillary thyroid carcinomas (CPTC). However, they have not been defined as a subtype of PTC, and their clinical characteristics have not been fully investigated.

The tumor size of PTC is important in clinical management and is used as an indicator for surgical treatment and a parameter for tumor–node–metastasis (TNM) classification (3). According to the American Thyroid Association (ATA) guidelines, total thyroidectomy and postoperative radioactive iodine (RAI) therapy are recommended for PTCs >4 cm in diameter because a larger tumor size is associated with an increased risk of metastasis and recurrence (3). However, we encountered CPTCs with good prognosis, even though they were extremely large. Kim et al. classified PTCs into cases with >50% and <50% cystic area and found no difference in the clinical stage and survival rate, albeit the significantly larger tumor diameter in cases with >50% cystic area (1). In this study, we aimed to clarify the clinical and pathological characteristics of CPTC and propose important indicators for its clinical management.

Materials and methods

Cystic papillary thyroid carcinoma

We reviewed data of 1199 patients with PTC who underwent resection and were histologically diagnosed at our institution between January and December 2010. After excluding patients with other malignant nodules >10 mm, 33 CPTC nodules (2.8%) were identified. CPTC was defined as a cystic area >50% of the tumor volume. The proportion of the cystic area was calculated by measuring the length of the whole tumor and the solid area in three directions on ultrasound images using the formula (Fig. 1). Whole tumor diameter (WTD; Fig. 1D) and solid area diameter (SAD; Fig. 1A) were defined as the maximum diameter in the three directions, and their mean (median, range) were 34.7 (30, 11–80) mm and 20.2 (20, 5–39) mm, respectively.

Figure 1
Figure 1

Ultrasound images of cystic papillary thyroid carcinoma (B-mode). To calculate the proportion of the cystic area, the lengths of the solid area (a–c), and the whole tumor (d–f) in the three directions were measured.

Citation: Endocrine Connections 13, 6; 10.1530/EC-24-0040

The following findings were obtained from the electronic medical records: age, sex, ultrasound and cytology reports, and postoperative course. The cytology reports were classified according to the Bethesda System for Reporting Thyroid Cytopathology (TBSRTC) (4). Pathological staging was based on the pathological TNM classification of the American Joint Committee on Cancer 8th Edition (5).

Control

We prepared two groups as controls: WTD of non-cystic PTC matched for WTD or SAD of CPTCs. The WTD-matched control (WTD-MC) consisted of 72 non-cystic PTC nodules resected between January and July 2010, and the SAD-matched control (SAD-MC) consisted of 71 non-cystic PTC nodules resected between January and March 2010. Both control cases were serially extracted and matched for WTD diameter after excluding the cases with another malignant nodules >10 mm. The mean (median) diameters of WTD-MCs and SAD-MCs were 33.0 (30) mm and 19.7 (19) mm, respectively.

Statistical analysis

Student’s t-test, Fisher’s direct probability test, Peason’s χ2 test, and log-rank test were used for statistical analyses, and a P < 0.05 was considered a significant difference.

The study protocol was reviewed and approved by the Institutional Review Board of Kuma Hospital (20231012-4) and was in accordance with the 1964 Helsinki Declaration and its amendments or comparable ethical standards. All subjects provided informed consent.

Results

Table 1 shows the clinical, ultrasonographic, and cytological findings of the examined patients with PTC. The mean age of the patients with CPTC was 55.2 years, with a female-to-male ratio of 2.0, which was not significantly different from that of WTD-MCs (53.6 years, 3.2), and significantly older and more prevalent in males than that of SAD-MCs (48.5 years, 6.1) (P < 0.05 and P < 0.05, respectively).

Table 1

Clinical, ultrasonographic, and cytological findings of the three groups of papillary thyroid carcinoma cases.

CPTC (n = 33) WTD-MC (n = 72) SAD-MC (n = 71) P
CPTC vs WTD-MC CPTC vs SAD-MC
Age mean (range) (years) 55.2 (18–82) 53.6 (12–9) 48.5 (20–83) NS 0.0479
Female/male ratio 2.0 3.2 6.1 NS 0.0346
Whole tumor diameter; mean (range) (mm) 34.7 (11–80) 33.0 (11–70) 19.7 (5–43)
Location
 Right lobe 27.3% (9) 45.8% (33) 40.8% (29) NS NS
 Isthmus 3.0% (1) 2.8% (2) 5.6% (4)
 Left lobe 39.4% (13) 51.4% (37) 53.5% (38)
Ultrasound report
 Low suspicion 15.2% (5) 4.2% (3) 0% (0) NS 0.0015
 Intermediate 15.2% (5) 6.9% (5) 8.5% (6)
 High suspicion 69.7% (23) 88.9% (64) 91.5% (65)
Cytological report
  I. Nondiagnostic 3.0% (1) 0% (0) 2.8% (2) NS NS
 II. Benign 3.0% (1) 2.9% (2) 4.2% (3)
 III. AUS 9.1% (3) 2.9% (2) 9.9% (7)
 IV. Follicular neoplasm 0% (0) 0% (0) 0% (0)
 V. SFM 3.0% (1) 8.6% (6) 8.5% (6)
 VI. Malignant 81.8% (27) 85.7% (60) 74.6% (53)
 Diagnostic accuracy (V+VI) 84.8% (28) 94.3% (66) 83.1% (59) NS NS
 Repeat aspiration rate in I+II+III 80.0% (4) 25.0% (1) 58.3% (7) NS NS

CPTC, cystic papillary thyroid carcinoma; MC, matched control; NS, not significant; SAD, solid area diameter; WTD, whole tumor diameter.

Of the 33 CPTC nodules, 9, 1, and 13 were located in the right, isthmus, and left lobes, respectively. In the 12 CPTC nodules (36.4%), solid areas were located on the tracheal side. Cystic areas occupied the tumor ranging from 51.3% to 91.7% (mean, 73.4%). Of the CPTCs, 69.7% were classified as highly suspicious on ultrasound. The prevalence was significantly lower than that in WTD-MCs (88.9%) and SAD-MCs (91.5%) (P < 0.05, P < 0.005, respectively).

Upon cytological examination, the nondiagnostic rates of CPTCs, WTD-MCs, and SAD-MCs were 3.0%, 0%, and 2.8%, respectively. Only one non-diagnostic case of CPTC was not due to cyst fluid but to poor cellularity. The cytological diagnostic accuracy of CPTCs was 84.8%. This was not significantly different from those of WTD-MCs (94.3%) and SAD-MCs (83.1%). Of the five CPTC nodules classified as nondiagnostic or atypia of undetermined significance, four (80.0%) underwent re-aspiration, and all were diagnosed as malignant. The re-aspiration rate was higher than that in WTD-MCs (25.0%) and SAD-MCs (58.3%), with no significant difference.

Table 2 shows the surgical, microscopic, and postoperative findings. Total thyroidectomy and lateral neck lymph node dissection were performed in 69.7% and 30.3% of CPTC cases, respectively. These frequencies were significantly lower than those in the WDT-MCs (91.7%, 56.9%) (P < 0.05, P < 0.05) and did not differ significantly from those in the SAD-MCs (76.1%, 25.4%). Postoperative RAI therapy was administered in 6.1% of CPTCs cases, 13.9% of WTD-MC cases, and 1.4% of SAD-MC cases, and no significant differences were found.

Table 2

Surgical, microscopic, and postoperative findings of three groups of papillary thyroid carcinomas.

CPTC (n = 33) WTD-MC (n = 72) SAD-MC (n = 71) P
CPTC vs WTD-MC CPTC vs SAD-MC
Surgical procedures
 Lobectomy 30.3% (10) 8.3% (6) 23.9% (17) 0.0291 NS
 Total thyroidectomy 69.7% (23) 91.7% (66) 76.1% (54)
Neck lymph node dissection
 Not done 0% (0) 1.4% (1) 1.4% (1) 0.0262 NS
 Central 69.7% (23) 41.7% (30) 73.2% (52)
 Central + lateral 30.3% (10) 56.9% (41) 25.4% (18)
Postoperative RAI therapy 6.1% (2) 13.9% (10) 1.4% (1) NS NS
Histological findings
 Invasion into surrounding tissue 54.5% (18)
 Granulation tissue 51.5% (17)
Subtype
 Conventional 97.0% (32) 94.4% (68) 95.8% (68) NS NS
 Follicular 0% (0) 4.2% (3) 4.2% (3)
 Macrofollicular 0% (0) 1.4% (1) 0% (0)
 Oncocytic 3.0% (1) 0% (0) 0% (0)
 Extrathyroidal extension 9.1% (3) 31.9% (23) 11.3% (8) 0.0118 NS
 Ki-67 labeling index n = 29 n = 67 n = 63
 <5% 86.2% (25) 62.7% (42) 84.1% (53) 0.0286 NS
 ≥5% 13.8% (4) 37.3% (25) 15.9% (10)
pTNM classification
pT
 1 42.4% (14) 19.4% (14) 62.0% (44) NS 0.0346
 2 24.2% (8) 40.3% (29) 25.4% (18)
 3 27.3% (9) 26.4% (19) 12.7% (9)
 4 6.1% (2) 13.9% (10) 0% (0)
pN
 0·X 48.5% (16) 22.2% (16) 46.5% (33) 0.0049 NS
 1a 30.3% (10) 25.0% (18) 33.8% (24)
 1b 21.2% (7) 52.8% (38) 19.7% (14)
M (at the time of surgery)
 0 100% (33) 97.2% (70) 100% (71) NS NS
 1 0% (0) 2.8% (2) 0% (0)
Postoperative outcomes
 Follow-up period mean (range) (years) 11.2 (2.7–13.7) 11.5 (2.3–13.8) 12.4 (2.4–13.8) NS NS
 Progression free survival rate (10 years) 90.9% 79.6% 95.8% NS NS
 Recurrence 9.1% (3) 19.4% (14) 2.8% (2) NS NS
 Distant metastasis 0% (0) 6.9% (5) lung 3, bone 2 1.4% (1) lung 1 NS NS
 Cause-specific death 0% (0) 4.2% (3) 0% (0) NS

CPTC, cystic papillary thyroid carcinoma; MC, matched control; NS, not significant; pTNM, pathological tumor-node-metastasis; RAI, radioactive iodine; SAD, solid area diameter; WTD, whole tumor diameter.

Microscopic examination revealed invasion into the surrounding normal thyroid tissue in 18 CPTC nodules (54.5%), all of which were present around the solid area (Fig. 2). Twelve of them (66.7%) were >30 mm in diameter, and the frequency was higher than that without invasion into the surrounding normal thyroid tissue (20.0%) (P < 0.05). Granulation tissue was present in 17 (51.5%) nodules, all of which were located on the cystic walls (Fig. 3A). No carcinoma cells were observed in granulation tissue. Meanwhile, 76.5% of CPTCs with granulation tissue were >30 mm in diameter, whereas the frequency was 12.5% in those without them (P < 0.01). In one patient, the granulation tissue extended into the anterior cervical muscle (Fig. 3B). Another patient exhibited a psammoma body in the granulation tissue (Fig. 3C).

Figure 2
Figure 2

Cystic papillary thyroid carcinoma. The carcinoma cells invade from the solid area to surrounding normal thyroid tissue. Black bar showed 200 μm (hematoxylin and eosin, 2×).

Citation: Endocrine Connections 13, 6; 10.1530/EC-24-0040

Figure 3
Figure 3

Cystic papillary thyroid carcinoma associated with granulation tissue. The granulation tissue is in intimate contact with the cystic wall (A) and extends into the anterior cervical muscle (B). A psammoma body is present without carcinoma cells (C). Black bar showed 200 μm (hematoxylin and eosin, A and B: 2×, C: 10×).

Citation: Endocrine Connections 13, 6; 10.1530/EC-24-0040

Thirty-two CPTCs (97.0%) were of the conventional type, and the remaining one was of the oncocytic subtype. The frequencies of CPTCs with extrathyroidal extension and Ki-67 labeling index ≥5% were 9.1% and 13.8%, respectively, and they were significantly lower than those in WTD-MC (31.9% and 37.3%) and not significantly different from those of SAD-MC (11.3% and 15.9%).

Among CPTCs, 6.1% were classified as pathological T4. This frequency was lower than that of WTD-MCs (13.9%) and higher than that of SAD-MCs (0%). CPTCs with pathological N1b accounted for 21.2%, which was lower than that of WTD-MCs (52.8%), and analogous to that of SAD-MCs (19.7%). No M1 cases were observed in the CPTC and SAD-MC cases, and two WTD-MC cases showed distant metastasis at the time of surgery. During the follow-up period, three (9.1%) of the 33 CPTC cases occurred in local recurrence. No cases of CPTC with distant metastasis or cause-specific deaths were observed. The incidence was not significantly different between the WTD-MC and SAD-MC cases. Figure 4 shows the Kaplan–Meier curves for disease-free survival. CPTC cases had longer progression-free survival than that of WTD-MCs and shorter than that of SAD-MCs, without significant differences.

Figure 4
Figure 4

The Kaplan–Meier curves for disease-free survival of three groups of papillary thyroid carcinoma cases. Log-rank test was used for statistical analyses, and a P < 0.05 was considered as a significant difference. CPTC, cystic papillary thyroid carcinoma; MC, matched control; SAD, solid area diameter; WTD, whole tumor diameter.

Citation: Endocrine Connections 13, 6; 10.1530/EC-24-0040

Discussion

Although there are many subtypes of PTC, CPTC has not been formally proposed, and its definition has not yet been determined. In this study, we defined CPTC as PTC in which >50% of the tumor volume was cystic. The same definition was used by Kim et al. and Henrichsen et al. (1, 2). We believe this criterion is simple, clear, and easy to apply. However, its acceptance as a subtype depends on the clinical characteristics.

The median age of patients with conventional PTC has been reported to be 47–50 years, with a proportion of males ranging from 25% to 27% (6, 7). Kim et al. reported that the mean age of patients with CPTC was 44.9 years, and males accounted for 42.9% of the cases (1). In this study, both the mean age (55.2 years) of patients with CPTC and the proportion of males (33.3%) tended to be higher than those with conventional PTC. Machens et al. reported that the mean tumor size of conventional PTC was 21 mm (7). The mean tumor size (34.7 mm) of the CPTCs that we studied was larger. However, these results may have been influenced by the exclusion of active surveillance of papillary microcarcinoma (3). Moreover, Kim et al. reported that the tumor size of CPTCs was significantly larger than that of PTC with cystic areas covering <50% (1). From these data, we believe that CPTC tended to be larger than non-cystic PTC.

The diagnostic accuracy of ultrasonography for PTC nodules is markedly high. Baek et al. reported that 95.9% of conventional PTC cases are suspected to be malignant (8). However, no study to date has been conducted on the diagnosis of CPTC using ultrasound examination. The present study demonstrated that ultrasound examination indicated malignancy in 69.7% of CPTCs, and its accuracy was significantly lower than that of WTD-MC (88.9%) and SAD-MC (91.5%). Notably, CPTCs are considered to be easily undervalued, which may be due to the presence of the cyst (9).

As with ultrasonography, we showed that the diagnostic accuracy (84.8%) of cytology for CPTCs was lower than that for WTD-MC (94.3%). However, this was higher than the diagnostic accuracy of conventional PTC (65–79%) reported in previous studies (10, 11, 12). The aspiration cytology of lesions with marked cystic changes can be difficult to diagnose because of low cellularity and degenerative changes (1, 4, 13). Therefore, TBSRTC advocates that specimens with only foam cells should be classified as non-diagnostic because the possibility of CPTC cannot be ruled out (4). However, no CPTC nodules were classified as non-diagnostic due to cyst fluid in this study. This is probably because aspiration is performed under ultrasound guidance in all cases, and a solid area is targeted (14).

The treatment strategy for thyroid cancer is determined by the TNM stage or risk classification (3, 15). Total thyroidectomy with lymph node dissection and postoperative RAI therapy is recommended for PTCs with high TNM stage and/or high risk. Kim et al. reported that all patients with CPTC underwent total thyroidectomy (1). In this study, total thyroidectomy and central and lateral neck lymph node dissections were performed in 69.7% and 30.3% of CPTC cases, respectively, which were significantly less frequent than those in WDT-MC (91.7% and 56.9%) and similar to those in SAD-MC (76.1% and 25.4%). Surgery for CPTC at our institution appears to be more conservative than the global standards. Nevertheless, the recurrence rate in our cases was 9.1%, which was considerably lower than the result (28.6%) reported by Kim et al. (1). We believe that our treatment strategy is reasonable and conclude that the surgical procedure for tumor size should be determined by SAD and not WDT.

No previous study has examined in detail the histological findings of CPTC. Our study clarified two characteristic findings of CPTC: invasion into the surrounding normal thyroid tissue around the solid area and granulation tissue around the cystic wall. Wada et al. reported a case of CPTC with adhesions to the anterior cervical muscle; however, no carcinoma invasion was observed at the adhesion site (16). We did not find viable carcinoma cells within the granulation tissue, although psammoma bodies were observed. These findings suggest that granulation tissue around the cyst was caused by leakage of cystic fluid due to microtrauma to the cystic wall; however, it is unclear whether it was spontaneous or caused by fine needle aspiration. Notably, granulation tissue is less likely a tumor invasion but simply an inflammatory change and can be mistaken intraoperatively for extrathyroidal extension.

Several factors, such as pathological subtypes, Ki-67 labeling index, TNM classification, progression-free survival, and postoperative events, have been reported to predict the aggressiveness of PTC (3, 5, 7, 17, 18). A large tumor is a well-known poor prognostic factor (7, 17). Tawil et al. reported that progression-free survival in conventional PTC decreased as tumor size increased (17). The cumulative risks of extrathyroidal growth, lymph node metastasis, and distant metastasis increase linearly with increasing tumor size (7). However, in a report by Kim et al., the tumor size in the CPTC group was significantly larger than that in the group with fewer cystic components; however, no significant difference was found in disease-free survival between the two groups (1). Carcangiu et al. reported that patients with CPTC had a significantly greater chance of being free of disease, and no patient died of the tumor (19). It was assumed that the negative correlation between tumor size and progression-free survival is not applicable to CPTC. In this study, the frequencies of the cases with pathological N1b, pathological extrathyroidal extension, and Ki-67 labeling index ≥5% in CPTCs were significantly lower than those in WTD-MCs and relatively similar to SAD-MCs. In addition, patients with CPTC tended to have longer progression-free survival than those with WTD-MCs and shorter than those with SAD-MCs. In the surgical strategy and prognosis of CPTC, the evaluation of tumor size is based on SAD rather than on WTD. Therefore, we argue that SAD and WTD should be measured in CPTC.

In conclusion, we defined CPTC as a PTC with a cystic area occupying more than 50% of its volume. CPTC tended to be underestimated on ultrasound examination. The granulation tissue around the cyst was attributed to the leakage of cystic fluid, and not by tumor invasion, but simply by inflammatory changes. In the surgical strategy and prognosis of CPTC, the evaluation of tumor size should be based on SAD rather than on WTD. Therefore, we argue that SAD and WTD should be measured in CPTC.

Declaration of interest

All authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the study reported.

Funding

This work did not receive any specific grant from any funding agency in the public, commercial or not-for-profit sector.

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    Wada M, Kurokawa T, Hosoi H, Kaneko Y, & Motohara T. A case of papillary thyroid carcinoma with a giant cyst in young man. Official Journal of the Japan Association of Endocrine Surgeons and the Japanese Society of Thyroid Surgery 2021 38 3236. (https://doi.org/10.11226/jaesjsts.38.1_32)

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    Hakim Tawil JA, Rojas MF, Santivañez JJ, León L, & Gonz´alez Devia D. Prognostic factors for recurrence in patients with papillary thyroid carcinoma. Ear, Nose, and Throat Journal 2023 1455613231158792. (https://doi.org/10.1177/01455613231158792)

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  • Figure 1

    Ultrasound images of cystic papillary thyroid carcinoma (B-mode). To calculate the proportion of the cystic area, the lengths of the solid area (a–c), and the whole tumor (d–f) in the three directions were measured.

  • Figure 2

    Cystic papillary thyroid carcinoma. The carcinoma cells invade from the solid area to surrounding normal thyroid tissue. Black bar showed 200 μm (hematoxylin and eosin, 2×).

  • Figure 3

    Cystic papillary thyroid carcinoma associated with granulation tissue. The granulation tissue is in intimate contact with the cystic wall (A) and extends into the anterior cervical muscle (B). A psammoma body is present without carcinoma cells (C). Black bar showed 200 μm (hematoxylin and eosin, A and B: 2×, C: 10×).

  • Figure 4

    The Kaplan–Meier curves for disease-free survival of three groups of papillary thyroid carcinoma cases. Log-rank test was used for statistical analyses, and a P < 0.05 was considered as a significant difference. CPTC, cystic papillary thyroid carcinoma; MC, matched control; SAD, solid area diameter; WTD, whole tumor diameter.

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    Wada M, Kurokawa T, Hosoi H, Kaneko Y, & Motohara T. A case of papillary thyroid carcinoma with a giant cyst in young man. Official Journal of the Japan Association of Endocrine Surgeons and the Japanese Society of Thyroid Surgery 2021 38 3236. (https://doi.org/10.11226/jaesjsts.38.1_32)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Hakim Tawil JA, Rojas MF, Santivañez JJ, León L, & Gonz´alez Devia D. Prognostic factors for recurrence in patients with papillary thyroid carcinoma. Ear, Nose, and Throat Journal 2023 1455613231158792. (https://doi.org/10.1177/01455613231158792)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Tang J, Gui C, Qiu S, & Wang M. The clinicopathological significance of Ki67 in papillary thyroid carcinoma: a suitable indicator? World Journal of Surgical Oncology 2018 16 100. (https://doi.org/10.1186/s12957-018-1384-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Carcangiu ML, Zampi G, Pupi A, Castagnoli A, & Rosai J. Papillary carcinoma of the thyroid: a clinicopathologic study of 241 cases treated at the University of Florence, Italy. Cancer 1985 55 805828. (https://doi.org/10.1002/1097-0142(19850215)55:4<805::aid-cncr2820550419>3.0.co;2-z)

    • PubMed
    • Search Google Scholar
    • Export Citation