Papillary thyroid microcarcinoma with and without nodal metastasis: A comparative analysis

Saleh Alqaryan; Hisham Almousa; Raed Almutairi; Ahmed Altuwaijri; Aseel Doubi; Zuhour Alqahtani; Mohammad Almayouf; Majed Albarrak; Mohammed Alessa; Saleh Aldhahri; Khalid Alqahtani

doi:10.15537/smj.2024.45.3.20230638

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1. Goldman L ADA
. Cecil medicine. 23rd ed. Philadelphia, PA: Saunders Elsevier Publishers; 2007.
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1. Pizzato M,
2. Li M,
3. Vignat J,
4. Laversanne M,
5. Singh D,
6. Vecchia CL, et al.
The epidemiological landscape of thyroid cancer worldwide: GLOBOCAN estimates for incidence and mortality rates in 2020. Lancet Diabetes Endocrinol 2022; 10: 264-272.
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1. Ferlay J,
2. Ervik M,
3. Lam F,
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5. Mery L,
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Global Cancer Observatory: cancer today. Lyon, France: International Agency for Research on Cancer. [Updated 2020; Cited 2023 Aug 18]. Available from: http://gco.iarc.fr/today/home.
4.↵
1. Cao Y,
2. Wang Z,
3. Gu J,
4. Hu F,
5. Qi Y,
6. Yin Q, et al.
Reproductive factors but not hormonal factors associated with thyroid cancer risk: a systematic review and meta-analysis. BioMed Res Int 2015: 103515.
5.↵
1. Fariduddin MM,
2. Syed W.
Hurthle cell thyroid carcinoma. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023.
6.↵
1. Jameson J,
2. Loscalzo J. LD.
Harrison’s Principles of Internal Medicine. 16th ed. Blacklick, USA, McGraw-Hill Publishers; 2012.
7.↵
1. Lombardi CP,
2. Bellantone R,
3. De Crea C,
4. Paladino NC,
5. Fadda G,
6. Salvatori M, et al.
Papillary thyroid microcarcinoma: extrathyroidal extension, lymph node metastases, and risk factors for recurrence in a high prevalence of goiter area. World J Surg 2010; 34: 1214-1221.
OpenUrl CrossRef PubMed Web of Science
8.↵
1. Mirallié E,
2. Visset J,
3. Sagan C,
4. Hamy A,
5. Le Bodic MF,
6. Paineau J.
Localization of cervical node metastasis of papillary thyroid carcinoma. World J Surg 1999; 23: 970-973; discussion 973-974.
OpenUrl CrossRef PubMed Web of Science
9.↵
1. Wada N,
2. Duh QY,
3. Sugino K,
4. Iwasaki H,
5. Kameyama K,
6. Mimura T, et al.
Lymph node metastasis from 259 papillary thyroid microcarcinomas: frequency, pattern of occurrence and recurrence, and optimal strategy for neck dissection. Ann Surg 2003; 237: 399-407.
OpenUrl CrossRef PubMed Web of Science
10.↵
1. Pereira JA,
2. Jimeno J,
3. Miquel J,
4. Iglesias M,
5. Munné A,
6. Sancho JJ, et al.
Nodal yield, morbidity, and recurrence after central neck dissection for papillary thyroid carcinoma. Surgery 2005; 138: 1095–100; discussion 1100-1101.
OpenUrl CrossRef PubMed Web of Science
11.↵
1. Machens A,
2. Hinze R,
3. Thomusch O,
4. Dralle H.
Pattern of nodal metastasis for primary and reoperative thyroid cancer. World J Surg 2002; 26: 22-28.
OpenUrl CrossRef PubMed Web of Science
12.↵
1. Cooper DS,
2. Doherty GM,
3. Haugen BR,
4. Kloos RT,
5. Lee SL, et al
American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009; 19: 1167–214.
OpenUrl CrossRef PubMed Web of Science
13.↵
1. Yang Z,
2. Heng Y,
3. Lin J,
4. Lu C,
5. Yu D,
6. Tao L, et al.
Nomogram for predicting central lymph node metastasis in papillary thyroid cancer: a retrospective cohort study of two clinical centers. Cancer Res Treat 2020; 52: 1010-1018.
OpenUrl
14.↵
1. Gu JH,
2. Zhao YN,
3. Xie RL,
4. Xu WJ,
5. You DL,
6. Zhao ZF, et al.
Analysis of risk factors for cervical lymph node metastasis of papillary thyroid microcarcinoma: a study of 268 patients. BMC Endocr Disord 2019; 19: 124.
OpenUrl
15.↵
1. Zhao C,
2. Jiang W,
3. Gao Y,
4. Niu W,
5. Zhang X,
6. Xin L.
Risk factors for lymph node metastasis (LNM) in patients with papillary thyroid microcarcinoma (PTMC): role of preoperative ultrasound. J Int Med Res 2017; 45: 1221-1230.
OpenUrl
16.
1. Chow SM,
2. Law SCK,
3. Chan JKC,
4. Au SK,
5. Yau S,
6. Lau WH.
Papillary microcarcinoma of the thyroid: prognostic significance of lymph node metastasis and multifocality. Cancer 2003; 98: 31-40.
OpenUrl CrossRef PubMed Web of Science
17.↵
1. Ito Y,
2. Tomoda C,
3. Uruno T,
4. Takamura Y,
5. Miya A,
6. Kobayashi K, et al.
Preoperative ultrasonographic examination for lymph node metastasis: usefulness when designing lymph node dissection for papillary microcarcinoma of the thyroid. World J Surg 2004; 28: 498-501.
OpenUrl CrossRef PubMed Web of Science
18.↵
1. Mao J,
2. Zhang Q,
3. Zhang H,
4. Zheng K,
5. Wang R,
6. Wang G.
Risk factors for lymph node metastasis in papillary thyroid carcinoma: a systematic review and meta-analysis. Front Endocrinol 2020; 11: 265.
OpenUrl
19.
1. Luo Y,
2. Zhao Y,
3. Chen K,
4. Shen J,
5. Shi J,
6. Lu S, et al.
Clinical analysis of cervical lymph node metastasis risk factors in patients with papillary thyroid microcarcinoma. J Endocrinol Invest 2019; 42: 227-236.
OpenUrl
20.
1. Gui CY,
2. Qiu SL,
3. Peng ZH,
4. Wang M.
Clinical and pathologic predictors of central lymph node metastasis in papillary thyroid microcarcinoma: a retrospective cohort study. J Endocrinol Invest 2018; 41: 403-409.
OpenUrl
21.↵
1. Xu Y,
2. Xu L,
3. Wang J.
Clinical predictors of lymph node metastasis and survival rate in papillary thyroid microcarcinoma: analysis of 3607 patients at a single institution. J Surg Res 2018; 221: 128-134.
OpenUrl
22.↵
1. Sheng L,
2. Shi J,
3. Han B,
4. Lv B,
5. Li L,
6. Chen B, et al.
Predicting factors for central or lateral lymph node metastasis in conventional papillary thyroid microcarcinoma. Am J Surg 2020; 220: 334-340.
OpenUrl
23.↵
1. Zheng X,
2. Peng C,
3. Gao M,
4. Zhi J,
5. Hou X,
6. Zhao J, et al.
Risk factors for cervical lymph node metastasis in papillary thyroid microcarcinoma: a study of 1,587 patients. Cancer Biol Med 2019; 16: 121-130.
OpenUrl Abstract/FREE Full Text
24.↵
1. Wang D,
2. Zhu J,
3. Deng C,
4. Yang Z,
5. Hu D,
6. Shu X, et al.
Preoperative and pathological predictive factors of central lymph node metastasis in papillary thyroid microcarcinoma. Auris Nasus Larynx 2022; 49: 690-696.
OpenUrl
25.↵
1. Wen X,
2. Wang B,
3. Jin Q,
4. Zhang W,
5. Qiu M.
Thyroid antibody status is associated with central lymph node metastases in papillary thyroid carcinoma patients with Hashimoto’s thyroiditis. Ann Surg Oncol 2019; 26: 1751-1758.
OpenUrl
26.
1. Karatzas T,
2. Vasileiadis I,
3. Zapanti E,
4. Charitoudis G,
5. Karakostas E,
6. Boutzios G.
Thyroglobulin antibodies as a potential predictive marker of papillary thyroid carcinoma in patients with indeterminate cytology. Am J Surg 2016; 212.
27.↵
1. Vasileiadis I,
2. Boutzios G,
3. Charitoudis G,
4. Koukoulioti E,
5. Karatzas T.
Thyroglobulin antibodies could be a potential predictive marker for papillary thyroid carcinoma. Ann Surg Oncol 2014; 21: 2725-2732.
OpenUrl CrossRef PubMed
28.↵
1. Jung CK,
2. Bychkov A,
3. Kakudo K.
Update from the 2022 World Health Organization classification of thyroid tumors: a standardized diagnostic approach. Endocrinol Metab (Seoul) 2022; 37: 703–718.
OpenUrl

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Keywords

[1] 1.↵
Goldman L ADA
. Cecil medicine. 23rd ed. Philadelphia, PA: Saunders Elsevier Publishers; 2007.

[2] Goldman L ADA

[3] 2.↵
Pizzato M,
Li M,
Vignat J,
Laversanne M,
Singh D,
Vecchia CL, et al.
The epidemiological landscape of thyroid cancer worldwide: GLOBOCAN estimates for incidence and mortality rates in 2020. Lancet Diabetes Endocrinol 2022; 10: 264-272.
OpenUrl

[4] Pizzato M,

[5] Li M,

[6] Vignat J,

[7] Laversanne M,

[8] Singh D,

[9] Vecchia CL, et al.

[10] 3.↵
Ferlay J,
Ervik M,
Lam F,
Colombet M,
Mery L,
Piñeros M, et al.
Global Cancer Observatory: cancer today. Lyon, France: International Agency for Research on Cancer. [Updated 2020; Cited 2023 Aug 18]. Available from: http://gco.iarc.fr/today/home.

[11] Ferlay J,

[12] Ervik M,

[13] Lam F,

[14] Colombet M,

[15] Mery L,

[16] Piñeros M, et al.

[17] 4.↵
Cao Y,
Wang Z,
Gu J,
Hu F,
Qi Y,
Yin Q, et al.
Reproductive factors but not hormonal factors associated with thyroid cancer risk: a systematic review and meta-analysis. BioMed Res Int 2015: 103515.

[18] Cao Y,

[19] Wang Z,

[20] Gu J,

[21] Hu F,

[22] Qi Y,

[23] Yin Q, et al.

[24] 5.↵
Fariduddin MM,
Syed W.
Hurthle cell thyroid carcinoma. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023.

[25] Fariduddin MM,

[26] Syed W.

[27] 6.↵
Jameson J,
Loscalzo J. LD.
Harrison’s Principles of Internal Medicine. 16th ed. Blacklick, USA, McGraw-Hill Publishers; 2012.

[28] Jameson J,

[29] Loscalzo J. LD.

[30] 7.↵
Lombardi CP,
Bellantone R,
De Crea C,
Paladino NC,
Fadda G,
Salvatori M, et al.
Papillary thyroid microcarcinoma: extrathyroidal extension, lymph node metastases, and risk factors for recurrence in a high prevalence of goiter area. World J Surg 2010; 34: 1214-1221.
OpenUrl CrossRef PubMed Web of Science

[31] Lombardi CP,

[32] Bellantone R,

[33] De Crea C,

[34] Paladino NC,

[35] Fadda G,

[36] Salvatori M, et al.

[37] 8.↵
Mirallié E,
Visset J,
Sagan C,
Hamy A,
Le Bodic MF,
Paineau J.
Localization of cervical node metastasis of papillary thyroid carcinoma. World J Surg 1999; 23: 970-973; discussion 973-974.
OpenUrl CrossRef PubMed Web of Science

[38] Mirallié E,

[39] Visset J,

[40] Sagan C,

[41] Hamy A,

[42] Le Bodic MF,

[43] Paineau J.

[44] 9.↵
Wada N,
Duh QY,
Sugino K,
Iwasaki H,
Kameyama K,
Mimura T, et al.
Lymph node metastasis from 259 papillary thyroid microcarcinomas: frequency, pattern of occurrence and recurrence, and optimal strategy for neck dissection. Ann Surg 2003; 237: 399-407.
OpenUrl CrossRef PubMed Web of Science

[45] Wada N,

[46] Duh QY,

[47] Sugino K,

[48] Iwasaki H,

[49] Kameyama K,

[50] Mimura T, et al.

[51] 10.↵
Pereira JA,
Jimeno J,
Miquel J,
Iglesias M,
Munné A,
Sancho JJ, et al.
Nodal yield, morbidity, and recurrence after central neck dissection for papillary thyroid carcinoma. Surgery 2005; 138: 1095–100; discussion 1100-1101.
OpenUrl CrossRef PubMed Web of Science

[52] Pereira JA,

[53] Jimeno J,

[54] Miquel J,

[55] Iglesias M,

[56] Munné A,

[57] Sancho JJ, et al.

[58] 11.↵
Machens A,
Hinze R,
Thomusch O,
Dralle H.
Pattern of nodal metastasis for primary and reoperative thyroid cancer. World J Surg 2002; 26: 22-28.
OpenUrl CrossRef PubMed Web of Science

[59] Machens A,

[60] Hinze R,

[61] Thomusch O,

[62] Dralle H.

[63] 12.↵
Cooper DS,
Doherty GM,
Haugen BR,
Kloos RT,
Lee SL, et al
American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009; 19: 1167–214.
OpenUrl CrossRef PubMed Web of Science

[64] Cooper DS,

[65] Doherty GM,

[66] Haugen BR,

[67] Kloos RT,

[68] Lee SL, et al

[69] 13.↵
Yang Z,
Heng Y,
Lin J,
Lu C,
Yu D,
Tao L, et al.
Nomogram for predicting central lymph node metastasis in papillary thyroid cancer: a retrospective cohort study of two clinical centers. Cancer Res Treat 2020; 52: 1010-1018.
OpenUrl

[70] Yang Z,

[71] Heng Y,

[72] Lin J,

[73] Lu C,

[74] Yu D,

[75] Tao L, et al.

[76] 14.↵
Gu JH,
Zhao YN,
Xie RL,
Xu WJ,
You DL,
Zhao ZF, et al.
Analysis of risk factors for cervical lymph node metastasis of papillary thyroid microcarcinoma: a study of 268 patients. BMC Endocr Disord 2019; 19: 124.
OpenUrl

[77] Gu JH,

[78] Zhao YN,

[79] Xie RL,

[80] Xu WJ,

[81] You DL,

[82] Zhao ZF, et al.

[83] 15.↵
Zhao C,
Jiang W,
Gao Y,
Niu W,
Zhang X,
Xin L.
Risk factors for lymph node metastasis (LNM) in patients with papillary thyroid microcarcinoma (PTMC): role of preoperative ultrasound. J Int Med Res 2017; 45: 1221-1230.
OpenUrl

[84] Zhao C,

[85] Jiang W,

[86] Gao Y,

[87] Niu W,

[88] Zhang X,

[89] Xin L.

[90] 16.
Chow SM,
Law SCK,
Chan JKC,
Au SK,
Yau S,
Lau WH.
Papillary microcarcinoma of the thyroid: prognostic significance of lymph node metastasis and multifocality. Cancer 2003; 98: 31-40.
OpenUrl CrossRef PubMed Web of Science

[91] Chow SM,

[92] Law SCK,

[93] Chan JKC,

[94] Au SK,

[95] Yau S,

[96] Lau WH.

[97] 17.↵
Ito Y,
Tomoda C,
Uruno T,
Takamura Y,
Miya A,
Kobayashi K, et al.
Preoperative ultrasonographic examination for lymph node metastasis: usefulness when designing lymph node dissection for papillary microcarcinoma of the thyroid. World J Surg 2004; 28: 498-501.
OpenUrl CrossRef PubMed Web of Science

[98] Ito Y,

[99] Tomoda C,

[100] Uruno T,

[101] Takamura Y,

[102] Miya A,

[103] Kobayashi K, et al.

[104] 18.↵
Mao J,
Zhang Q,
Zhang H,
Zheng K,
Wang R,
Wang G.
Risk factors for lymph node metastasis in papillary thyroid carcinoma: a systematic review and meta-analysis. Front Endocrinol 2020; 11: 265.
OpenUrl

[105] Mao J,

[106] Zhang Q,

[107] Zhang H,

[108] Zheng K,

[109] Wang R,

[110] Wang G.

[111] 19.
Luo Y,
Zhao Y,
Chen K,
Shen J,
Shi J,
Lu S, et al.
Clinical analysis of cervical lymph node metastasis risk factors in patients with papillary thyroid microcarcinoma. J Endocrinol Invest 2019; 42: 227-236.
OpenUrl

[112] Luo Y,

[113] Zhao Y,

[114] Chen K,

[115] Shen J,

[116] Shi J,

[117] Lu S, et al.

[118] 20.
Gui CY,
Qiu SL,
Peng ZH,
Wang M.
Clinical and pathologic predictors of central lymph node metastasis in papillary thyroid microcarcinoma: a retrospective cohort study. J Endocrinol Invest 2018; 41: 403-409.
OpenUrl

[119] Gui CY,

[120] Qiu SL,

[121] Peng ZH,

[122] Wang M.

[123] 21.↵
Xu Y,
Xu L,
Wang J.
Clinical predictors of lymph node metastasis and survival rate in papillary thyroid microcarcinoma: analysis of 3607 patients at a single institution. J Surg Res 2018; 221: 128-134.
OpenUrl

[124] Xu Y,

[125] Xu L,

[126] Wang J.

[127] 22.↵
Sheng L,
Shi J,
Han B,
Lv B,
Li L,
Chen B, et al.
Predicting factors for central or lateral lymph node metastasis in conventional papillary thyroid microcarcinoma. Am J Surg 2020; 220: 334-340.
OpenUrl

[128] Sheng L,

[129] Shi J,

[130] Han B,

[131] Lv B,

[132] Li L,

[133] Chen B, et al.

[134] 23.↵
Zheng X,
Peng C,
Gao M,
Zhi J,
Hou X,
Zhao J, et al.
Risk factors for cervical lymph node metastasis in papillary thyroid microcarcinoma: a study of 1,587 patients. Cancer Biol Med 2019; 16: 121-130.
OpenUrl Abstract/FREE Full Text

[135] Zheng X,

[136] Peng C,

[137] Gao M,

[138] Zhi J,

[139] Hou X,

[140] Zhao J, et al.

[141] 24.↵
Wang D,
Zhu J,
Deng C,
Yang Z,
Hu D,
Shu X, et al.
Preoperative and pathological predictive factors of central lymph node metastasis in papillary thyroid microcarcinoma. Auris Nasus Larynx 2022; 49: 690-696.
OpenUrl

[142] Wang D,

[143] Zhu J,

[144] Deng C,

[145] Yang Z,

[146] Hu D,

[147] Shu X, et al.

[148] 25.↵
Wen X,
Wang B,
Jin Q,
Zhang W,
Qiu M.
Thyroid antibody status is associated with central lymph node metastases in papillary thyroid carcinoma patients with Hashimoto’s thyroiditis. Ann Surg Oncol 2019; 26: 1751-1758.
OpenUrl

[149] Wen X,

[150] Wang B,

[151] Jin Q,

[152] Zhang W,

[153] Qiu M.

[154] 26.
Karatzas T,
Vasileiadis I,
Zapanti E,
Charitoudis G,
Karakostas E,
Boutzios G.
Thyroglobulin antibodies as a potential predictive marker of papillary thyroid carcinoma in patients with indeterminate cytology. Am J Surg 2016; 212.

[155] Karatzas T,

[156] Vasileiadis I,

[157] Zapanti E,

[158] Charitoudis G,

[159] Karakostas E,

[160] Boutzios G.

[161] 27.↵
Vasileiadis I,
Boutzios G,
Charitoudis G,
Koukoulioti E,
Karatzas T.
Thyroglobulin antibodies could be a potential predictive marker for papillary thyroid carcinoma. Ann Surg Oncol 2014; 21: 2725-2732.
OpenUrl CrossRef PubMed

[162] Vasileiadis I,

[163] Boutzios G,

[164] Charitoudis G,

[165] Koukoulioti E,

[166] Karatzas T.

[167] 28.↵
Jung CK,
Bychkov A,
Kakudo K.
Update from the 2022 World Health Organization classification of thyroid tumors: a standardized diagnostic approach. Endocrinol Metab (Seoul) 2022; 37: 703–718.
OpenUrl

[168] Jung CK,

[169] Bychkov A,

[170] Kakudo K.

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A comparative analysis

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Papillary thyroid microcarcinoma with and without nodal metastasis

A comparative analysis

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