Clinical value of ultrasonographic features in predicting tumor growth of papillary thyroid microcarcinoma during active surveillance_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

 YUE Can ¹ , HU Haiping ² , JIANG Yong ³ , SHANG Lei ¹ ,  MA Buyun ¹

1. Department of Ultrasound Medicine, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;
2. Department of Ultrasound Medicine, Sichuan Longchang People’s Hospital, Longchang, Sichuan 642150, P. R. China;
3. Department of Pathology, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding?author：

MA Buyun, Email: ws_mby@126.com

Keywords：

papillary thyroid microcarcinoma; active surveillance; ultrasound; nodule growth

DOI：

10.7507/1007-9424.202102044

Video：

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Objective To explore the value of active surveillance (AS) with ultrasound for papillary thyroid microcarcinoma (PTMC) tumor growth.Methods A retrospective collection of 196 patients who underwent ultrasound-guided fine-needle aspiration biopsy at West China Hospital of Sichuan University from January 2014 to December 2018 were pathologically diagnosed as PTMC, and no cervical lymph node metastasis was found on ultrasound, and AS was performed. According to the change of the maximum diameter of the nodule, the patients were divided into the maximum diameter increase group, the maximum diameter stable group and the maximum diameter reduction group. According to the nodule volume change, the patients were divided into the volume increase group, the volume stable group and the volume reduction group. The differences in the patients’ gender, age, with Hashimoto’s thyroiditis, follow-up time, tumor size, boundary, shape, echo, aspect ratio, calcifications, multifocality, bilateral involvement, other nodule, surrounding tissues and cervical lymph nodes among the different groups were analyzed in order to clarify the related factors of tumor growth.Results One hundred and ninety-six patients had ultrasound AS time ranging from 6 to 79 months with the median (quartile) time were 16.0 (10.0, 30.0) months. One hundred and seventeen patients (59.7%) were in AS for 6 to 63 months with the median (quartile) time were 13.0. (8.0, 22.0), surgical treatments were performed after termination of AS. Forty-five patients (23.0%) continued to perform AS, 34 patients (17.3%) did not continue to perform AS in West China Hospital of Sichuan University. There was no significant reduction in the maximum diameter and volume of the nodules in all cases. Among them, 9 cases (4.6%) had an increase in the maximum diameter of the nodules, and 187 cases (95.4%) had a stable maximum diameter. Forty cases (20.4%) had an increase in the volume of the nodules, and 156 cases (79.6%) had a stable volume of the nodules. Comparison of the maximum diameter change of nodules between the two groups, there was a significant difference in the age of patients (P<0.05). Comparison of the maximum volume change between the two groups, there were significant differences in age, follow-up time and initial nodule volume (P<0.05). Logistic regression analysis showed that younger age was an independent risk factor for PTMC nodule growth [OR＝0.638, 95%CI (0.601, 0.675), P＝0.015].Conclusions Younger age is a risk factor for PTMC tumor growth. We should adopt a more active monitoring program for younger patients. The increase of PTMC tumor volume can be more easily monitored than the increase of its maximum diameter, so it can be used as an indicator to predict nodule growth at an earlier stage in AS.

Citation： YUE Can, HU Haiping, JIANG Yong, SHANG Lei, MA Buyun. Clinical value of ultrasonographic features in predicting tumor growth of papillary thyroid microcarcinoma during active surveillance. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(10): 1294-1300. doi: 10.7507/1007-9424.202102044 Copy

1.	Miranda-Filho A, Lortet-Tieulent A, Bray F, et al. Thyroid cancer incidence trends by histology in 25 countries: a population-based study. Lancet Diabetes Endocrinol, 2021, 9(4): 225-234.
2.	Liu YH, Lai FH, Long JY, et al. Screening and the epidemic of thyroid cancer in China: An analysis of national representative inpatient and commercial insurance databases. Int J Cancer, 2021, 148(5): 1106-1114.
3.	Morris LG, Tuttle RM, Davies L. Changing trends in the incidence of thyroid cancer in the United States. JAMA Otolaryngol Head Neck Surg, 2016, 142(7): 709-711.
4.	Ku?cu O, ?nay ?, Kayahan B, et al. The rising incidence of papillary thyroid microcarcinoma and is completion surgery necessary or not? Otolaryngol Pol, 2016, 70(3): 15-19.
5.	中國抗癌協會甲狀腺癌專業委員會(CATO). 甲狀腺微小乳頭狀癌診斷與治療中國專家共識(2016版). 中國腫瘤臨床, 2016, 43(10): 405-411.
6.	La Vecchia C, Malvezzi M, Bosetti C, et al. Thyroid cancer mortality and incidence: A global overview. Int J Cancer, 2015, 136(9): 2187-2195.
7.	董芬, 張彪, 單廣良. 中國甲狀腺癌的流行現狀和影響因素. 中國癌癥雜志, 2016, 26(1): 47-52.
8.	中華人民共和國國家衛生健康委員會. 甲狀腺癌診療規范(2018年版). 中華普通外科學文獻(電子版), 2019, 13(1): 1-15.
9.	畢鐵強. 甲狀腺微小乳頭狀癌的診治現狀與思考. 中國腫瘤外科雜志, 2018, 10(6): 341-346.
10.	Welch HG, Doherty GM. Saving thyroids—overtreatment of small papillary cancers. N Engl J Med, 2018, 379(4): 310-312.
11.	Vaccarella S, Franceschi S, Bray F, et al. Worldwide thyroid-cancer epidemic? The increasing impact of overdiagnosis. N Engl J Med, 2016, 375(7): 614-617.
12.	Jeon MJ, Kim WG, Choi YM, et al. Features predictive of distant metastasis in papillary thyroid microcarcinomas. Thyroid, 2016, 26(1): 161-168.
13.	Ross DS, Litofsky D, Ain KB, et al. Recurrence after treatment of micropapillary thyroid cancer. Thyroid, 2009, 19(10): 1043-1048.
14.	Siddiqui S, White MG, Antic T, et al. Clinical and pathologic predictors of lymph node metastasis and recurrence in papillary thyroid microcarcinoma. Thyroid, 2016, 26(6): 807-815.
15.	Chang YW, Kim HS, Kim HY, et al. Should central lymph node dissection be considered for all papillary thyroid microcarcinoma? Asian J Surg, 2016, 39(4): 197-201.
16.	Galofré JC. The dilemma of papillary thyroid microcarcinoma management. To operate or not to operate, that is the question. Endocrinol Diabetes Nutr, 2019, 66(8): 469-471.
17.	Haugen BR, Alexander EK, Bible KC, et al. 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, 2016, 26(1): 1-133.
18.	Leboulleux S, Tuttle RM, Pacini F, et al. Papillary thyroid microcarcinoma: Time to shift from surgery to active surveillance? Lancet Diabetes Endocrinol, 2016, 4(11): 933-942.
19.	Chen RC, Rumble RB, Loblaw DA, et al. Active surveillance for the management of localized prostate cancer (Cancer Care Ontario Guideline): American Society of Clinical Oncology Clinical Practice Guideline Endorsement. J Clin Oncol, 2016, 34(18): 2182-2190.
20.	侯慶, 陳宇, 馬步云, 等. 超聲評估甲狀腺結節內不同鈣化類型的臨床研究. 西部醫學, 2016, 28(9): 1297-1301.
21.	Oh EM, Chung YS, Song WJ, et al. The pattern and significance of the calcifications of papillary thyroid microcarcinoma presented in preoperative neck ultrasonography. Ann Surg Treat Res, 2014, 86(3): 115-121.
22.	Ito Y, Fukushima M, Higashiyama T, et al. Tumor size is the strongest predictor of microscopic lymph node metastasis and lymph node recurrence of N0 papillary thyroid carcinoma. Endocr J, 2013, 60(1): 113-117.
23.	Zhao Q, Ming J, Liu C, et al. Multifocality and total tumor diameter predict central neck lymph node metastases in papillary thyroid microcarcinoma. Ann Surg Oncol, 2013, 20(3): 746-752.
24.	Ito Y, Miyauchi A, Kihara M, et al. Patient age is significantly related to the progression of papillary microcarcinoma of the thyroid under observation. Thyroid, 2014, 24(1): 27-34.
25.	Kwon H, Oh HS, Kim M, et al. Active surveillance for patients with papillary thyroid microcarcinoma: A single center’s experience in Korea. J Clin Endocrinol Metab, 2017, 102(6): 1917-1925.
26.	Lin JF, Jonker PKC, Cunich M, et al. Surgery alone for papillary thyroid microcarcinoma is less costly and more effective than long term active surveillance. Surgery, 2020, 167(1): 110-116.
27.	Liu Z, Huang T. Papillary thyroid microcarcinoma and active surveillance. Lancet Diabetes Endocrinol, 2016, 4(12): 974-975.
28.	Tuttle RM, Fagin JA, Minkowitz G, et al. Natural history and tumor volume kinetics of papillary thyroid cancers during active surveillance. JAMA Otolaryngol Head Neck Surg, 2017, 143(10): 1015-1020.
29.	Oh HS, Kwon H, Song E, et al. Tumor volume doubling time in active surveillance of papillary thyroid carcinoma. Thyroid, 2019, 29(5): 642-649.
30.	Cho SY, Lee TH, Ku YH, et al. Central lymph node metastasis in papillary thyroid microcarcinoma can be stratified according to the number, the size of metastatic foci, and the presence of desmoplasia. Surgery, 2015, 157(1): 111-118.
31.	Mehanna H, Al-Maqbili T, Carter B, et al. Differences in the recurrence and mortality outcomes rates of incidental and nonincidental papillary thyroid microcarcinoma: A systematic review and meta-analysis of 21 329 person-years of follow-up. J Clin Endocrinol Metab, 2014, 99(8): 2834-2843.
32.	Sugitani I, Toda K, Yamada K, et al. Three distinctly different kinds of papillary thyroid microcarcinoma should be recognized: Our treatment strategies and outcomes. World J Surg, 2010, 34(6): 1222-1231.
33.	Oda H, Miyauchi A, Ito Y, et al. Incidences of unfavorable events in the management of low-risk papillary microcarcinoma of the thyroid by active surveillance versus immediate surgery. Thyroid, 2016, 26(1): 150-155.
34.	錢凱, 孫團起, 郭凱, 等. 甲狀腺微小乳頭狀癌密切隨訪標準的回顧性對比研究. 中華耳鼻喉頭頸外科雜志, 2017, 52(6): 430-434.
35.	Sasaki T, Miyauchi A, Ito Y, et al. Marked decrease over time in conversion surgery after active surveillance of low-risk papillary thyroid microcarcinoma. Thyroid, 2021, 31(2): 217-223.
36.	Park AY, Kim JA, Son EJ, et al. Shear-wave elastography for papillary thyroid carcinoma can improve prediction of cervical lymph node metastasis. Ann Surg Oncol, 2016, 23(Suppl 5): 722-729.
37.	樊金芳, 陶玲玲, 詹維偉, 等. 超聲造影和彈性成像對甲狀腺微小乳頭狀癌頸部中央區淋巴結轉移的價值. 醫學影像學雜志, 2020, 30(9): 1582-1586.

1. Miranda-Filho A, Lortet-Tieulent A, Bray F, et al. Thyroid cancer incidence trends by histology in 25 countries: a population-based study. Lancet Diabetes Endocrinol, 2021, 9(4): 225-234.
2. Liu YH, Lai FH, Long JY, et al. Screening and the epidemic of thyroid cancer in China: An analysis of national representative inpatient and commercial insurance databases. Int J Cancer, 2021, 148(5): 1106-1114.
3. Morris LG, Tuttle RM, Davies L. Changing trends in the incidence of thyroid cancer in the United States. JAMA Otolaryngol Head Neck Surg, 2016, 142(7): 709-711.
4. Ku?cu O, ?nay ?, Kayahan B, et al. The rising incidence of papillary thyroid microcarcinoma and is completion surgery necessary or not? Otolaryngol Pol, 2016, 70(3): 15-19.
5. 中國抗癌協會甲狀腺癌專業委員會(CATO). 甲狀腺微小乳頭狀癌診斷與治療中國專家共識(2016版). 中國腫瘤臨床, 2016, 43(10): 405-411.
6. La Vecchia C, Malvezzi M, Bosetti C, et al. Thyroid cancer mortality and incidence: A global overview. Int J Cancer, 2015, 136(9): 2187-2195.
7. 董芬, 張彪, 單廣良. 中國甲狀腺癌的流行現狀和影響因素. 中國癌癥雜志, 2016, 26(1): 47-52.
8. 中華人民共和國國家衛生健康委員會. 甲狀腺癌診療規范(2018年版). 中華普通外科學文獻(電子版), 2019, 13(1): 1-15.
9. 畢鐵強. 甲狀腺微小乳頭狀癌的診治現狀與思考. 中國腫瘤外科雜志, 2018, 10(6): 341-346.
10. Welch HG, Doherty GM. Saving thyroids—overtreatment of small papillary cancers. N Engl J Med, 2018, 379(4): 310-312.
11. Vaccarella S, Franceschi S, Bray F, et al. Worldwide thyroid-cancer epidemic? The increasing impact of overdiagnosis. N Engl J Med, 2016, 375(7): 614-617.
12. Jeon MJ, Kim WG, Choi YM, et al. Features predictive of distant metastasis in papillary thyroid microcarcinomas. Thyroid, 2016, 26(1): 161-168.
13. Ross DS, Litofsky D, Ain KB, et al. Recurrence after treatment of micropapillary thyroid cancer. Thyroid, 2009, 19(10): 1043-1048.
14. Siddiqui S, White MG, Antic T, et al. Clinical and pathologic predictors of lymph node metastasis and recurrence in papillary thyroid microcarcinoma. Thyroid, 2016, 26(6): 807-815.
15. Chang YW, Kim HS, Kim HY, et al. Should central lymph node dissection be considered for all papillary thyroid microcarcinoma? Asian J Surg, 2016, 39(4): 197-201.
16. Galofré JC. The dilemma of papillary thyroid microcarcinoma management. To operate or not to operate, that is the question. Endocrinol Diabetes Nutr, 2019, 66(8): 469-471.
17. Haugen BR, Alexander EK, Bible KC, et al. 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, 2016, 26(1): 1-133.
18. Leboulleux S, Tuttle RM, Pacini F, et al. Papillary thyroid microcarcinoma: Time to shift from surgery to active surveillance? Lancet Diabetes Endocrinol, 2016, 4(11): 933-942.
19. Chen RC, Rumble RB, Loblaw DA, et al. Active surveillance for the management of localized prostate cancer (Cancer Care Ontario Guideline): American Society of Clinical Oncology Clinical Practice Guideline Endorsement. J Clin Oncol, 2016, 34(18): 2182-2190.
20. 侯慶, 陳宇, 馬步云, 等. 超聲評估甲狀腺結節內不同鈣化類型的臨床研究. 西部醫學, 2016, 28(9): 1297-1301.
21. Oh EM, Chung YS, Song WJ, et al. The pattern and significance of the calcifications of papillary thyroid microcarcinoma presented in preoperative neck ultrasonography. Ann Surg Treat Res, 2014, 86(3): 115-121.
22. Ito Y, Fukushima M, Higashiyama T, et al. Tumor size is the strongest predictor of microscopic lymph node metastasis and lymph node recurrence of N0 papillary thyroid carcinoma. Endocr J, 2013, 60(1): 113-117.
23. Zhao Q, Ming J, Liu C, et al. Multifocality and total tumor diameter predict central neck lymph node metastases in papillary thyroid microcarcinoma. Ann Surg Oncol, 2013, 20(3): 746-752.
24. Ito Y, Miyauchi A, Kihara M, et al. Patient age is significantly related to the progression of papillary microcarcinoma of the thyroid under observation. Thyroid, 2014, 24(1): 27-34.
25. Kwon H, Oh HS, Kim M, et al. Active surveillance for patients with papillary thyroid microcarcinoma: A single center’s experience in Korea. J Clin Endocrinol Metab, 2017, 102(6): 1917-1925.
26. Lin JF, Jonker PKC, Cunich M, et al. Surgery alone for papillary thyroid microcarcinoma is less costly and more effective than long term active surveillance. Surgery, 2020, 167(1): 110-116.
27. Liu Z, Huang T. Papillary thyroid microcarcinoma and active surveillance. Lancet Diabetes Endocrinol, 2016, 4(12): 974-975.
28. Tuttle RM, Fagin JA, Minkowitz G, et al. Natural history and tumor volume kinetics of papillary thyroid cancers during active surveillance. JAMA Otolaryngol Head Neck Surg, 2017, 143(10): 1015-1020.
29. Oh HS, Kwon H, Song E, et al. Tumor volume doubling time in active surveillance of papillary thyroid carcinoma. Thyroid, 2019, 29(5): 642-649.
30. Cho SY, Lee TH, Ku YH, et al. Central lymph node metastasis in papillary thyroid microcarcinoma can be stratified according to the number, the size of metastatic foci, and the presence of desmoplasia. Surgery, 2015, 157(1): 111-118.
31. Mehanna H, Al-Maqbili T, Carter B, et al. Differences in the recurrence and mortality outcomes rates of incidental and nonincidental papillary thyroid microcarcinoma: A systematic review and meta-analysis of 21 329 person-years of follow-up. J Clin Endocrinol Metab, 2014, 99(8): 2834-2843.
32. Sugitani I, Toda K, Yamada K, et al. Three distinctly different kinds of papillary thyroid microcarcinoma should be recognized: Our treatment strategies and outcomes. World J Surg, 2010, 34(6): 1222-1231.
33. Oda H, Miyauchi A, Ito Y, et al. Incidences of unfavorable events in the management of low-risk papillary microcarcinoma of the thyroid by active surveillance versus immediate surgery. Thyroid, 2016, 26(1): 150-155.
34. 錢凱, 孫團起, 郭凱, 等. 甲狀腺微小乳頭狀癌密切隨訪標準的回顧性對比研究. 中華耳鼻喉頭頸外科雜志, 2017, 52(6): 430-434.
35. Sasaki T, Miyauchi A, Ito Y, et al. Marked decrease over time in conversion surgery after active surveillance of low-risk papillary thyroid microcarcinoma. Thyroid, 2021, 31(2): 217-223.
36. Park AY, Kim JA, Son EJ, et al. Shear-wave elastography for papillary thyroid carcinoma can improve prediction of cervical lymph node metastasis. Ann Surg Oncol, 2016, 23(Suppl 5): 722-729.
37. 樊金芳, 陶玲玲, 詹維偉, 等. 超聲造影和彈性成像對甲狀腺微小乳頭狀癌頸部中央區淋巴結轉移的價值. 醫學影像學雜志, 2020, 30(9): 1582-1586.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Clinical value of ultrasonographic features in predicting tumor growth of papillary thyroid microcarcinoma during active surveillance

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