Skip to main content
Download PDF

The effect of chronic lymphocytic thyroiditis on patients with thyroid cancer

World Journal of Surgical Oncology volume 12, Article number: 277 (2014) Cite this article

Abstract

Background

The purpose of this study was to investigate the association between chronic lymphocytic thyroiditis (CLT) and malignant tumors of the thyroid.

Methods

A retrospective review of 647 patients who underwent thyroid surgery at the Department of Breast and Thyroid Surgery in Anhui Provincial Hospital, China in 2012 was performed. The clinicopathological characteristics of patients with thyroid malignancies and CLT were collected. CLT was diagnosed by histopathological method.

Results

Among 647 patients, 144 patients had thyroid malignancies and 108 patients had been diagnosed with CLT. Moreover, in total, 44 patients had thyroid malignancies coexistent with CLT: forty-one (93.2%) patients had been diagnosed with the papillary thyroid cancer (PTC); two (4.5%) patients suffered from medullary carcinoma; and one (2.3%) patient suffered from lymphoma. The morbidity of thyroid malignancies in patients with CLT was significantly higher than that in patients without CLT (40.7% versus 18.6%; P <0.001). A female preponderance was observed in the patients with CLT compared with those without CLT (P <0.001). There was no statistically significant difference in the tumor size (P = 0.073), multifocality (P = 0.0871), neck lymph node metastasis (P = 0.350), age (P = 0.316), microcarcinoma (P = 0.983) and tumor-node-metastasis (TNM) stage (P = 0.949) between the patients of thyroid malignancies with CLT and without CLT.

Conclusions

Female predominance was observed in patients with CLT. CLT may have no effect on the progression of thyroid malignant tumor. Nevertheless, the influences of CLT on the prognosis of the thyroid carcinoma still need to be investigated with a larger sample size.

Background

Thyroid cancer is the most common endocrine malignancy and occurs in 8.7 per 100 000 individuals in the United States, accounting for approximately 1% of all cancers[1–3]. It has been reported that clinicopathologic factors, such as sex, age, tumor size, multifocality, extrathyroidal extension and lymph node metastasis, are related to the prognosis of thyroid cancers[4–6]. Different morphological types of thyroid cancer mainly include papillary thyroid carcinoma (PTC), follicular carcinoma, medullary carcinoma, anaplastic carcinoma and thyroid lymphoma. PTC is the most prevalent manifestation of thyroid cancer. It represents 70 to 80% of all diagnosed thyroid cancers[7]. Thyroid lymphoma is a rare thyroid malignant tumor, accounting for 1 to 5% of all thyroid malignancies and less than 2% of extranodal lymphomas[8].

Chronic lymphocytic thyroiditis (CLT, or Hashimoto's thyroiditis (HT)) has been recognized as a common autoimmune thyroid disorder in which the thyroid gland is attacked by various antibody and cell-mediated immune processes[9]. The clinical and pathologic associations between CLT and thyroid epithelial neoplasms were first described by Dailey et al. in 1955[10]. Studies have found that CLT can coexist with other autoimmune thyroid diseases and thyroid malignancies[11, 12]. A well-established association that patients with CLT have an increased risk of thyroid lymphoma and PTC has been proposed[13–16]. In addition, Okayasu et al.[17] revealed an association between CLT and PTC in the Japanese, and in white and African American populations, and also indicated that the possibility of CLT as a predisposing factor for PTC. However, the association between PTC and CLT with regard to pathogenesis and prognostic outcomes of their co-occurrence remains unclear among Chinese population; furthermore, the association between the other types of thyroid cancers and CLT still needs to be studied.

In this present study, we aimed to evaluate the presence of coexistent CLT in a population of patients who underwent thyroid surgery at the Department of Breast and Thyroid Surgery in Anhui Provincial Hospital, China. Then the association of CLT with clinicopathological parameters including age, sex, tumor size, multifocality, neck lymph node metastasis, microcarcinoma and TNM stage of patients with thyroid malignancies was determined.

Methods

Patients

In 2012, 647 patients who had undergone thyroid surgery at the Department of Breast and Thyroid Surgery in Anhui Provincial Hospital, China were enrolled in this study. All participants gave written informed consents at the time of surgery to allow future reviewing of medical records, and this retrospective study was approved by the hospital medical ethics committee.

Diagnosis of chronic lymphocytic thyroiditis

The histopathological manifestations of CLT include diffuse lymphoplasmacytic and plasma cell infiltration, lymphoid follicle formation with germinal centers, varying degrees of fibrosis, parenchymal atrophy in the area of normal thyroid tissue, and the presence of large follicular cells with abundant oxyphilic cells. Only the presence of peri-tumoral lymphocytic infiltration was not considered as CLT[18–20].

Data collection

The general characteristics of the patients with thyroid malignancies were recorded, including age, sex and cancer types. The clinicopathological parameters, such as tumor size, multifocality, neck lymph node metastasis, microcarcinoma and TNM stage, of patients with thyroid malignancies and with and without CLT were collected to analyze the effect of coexistent CLT in the patients with thyroid cancers.

Meanwhile, the serological examination results, preoperative ultrasonographic examination results and surgical methods of patients of thyroid malignancies with coexistent CLT were collected.

Statistical analysis

Statistical analysis was performed by SPSS 11.5 software (SPSS, Chicago, IL, USA). The measurement data were expressed as mean ± standard deviation and analyzed by t-test. The chi-square (χ2) test was used to analyze the enumeration data. There is significantly statistical difference when P <0.05.

Results

General characteristics of patients with thyroid malignancies

The general characteristics of patients with thyroid malignancies are shown in Table 1. Among the 647 patients who underwent thyroid surgery, there were 144 patients (female/male: 106/38; 46.9 ± 13.9 years) with thyroid malignancies, 108 patients (female/male: 101/7) with CLT and 395 with other thyroid diseases. Moreover, 44 patients (female/male: 41/3; 43.3 ± 13.2 years) with thyroid malignancies had co-existing CLT. Among them, 41 patients had been diagnosed with papillary carcinoma, 2 patients suffered from medullary carcinoma and 1 patient developed lymphoma.

Table 1 The general characteristics of patients with thyroid malignancies and the morbidity of malignancy of patients with or without chronic lymphocytic thyroiditis (CLT)
Full size table

Comparison of morbidity of malignancy between patients with and without chronic lymphocytic thyroiditis

Comparison of morbidity of malignancy between patients with and without CLT were shown in Table 1. Thyroid malignancies were detected in 44 (40.7%) of the 108 patients with CLT and 100 (18.6%) of the 539 patients without CLT. The morbidity of thyroid malignancies between patients with CLT was significantly higher than patients without CLT (P <0.001).

Clinicopathological parameters of patients with and without chronic lymphocytic thyroiditis

The differences in clinicopathological parameters between patients with and without CLT were analyzed in Table 2. The 144 patients with thyroid malignancies were mainly at stage I (83/144, 57.6%) and stage II (34/144, 23.6%). There was no statistically significant difference in the tumor size (P = 0.073), multifocality (P = 0.0871), neck lymph node metastasis (P = 0.350), age (P = 0.316), microcarcinoma (P = 0.983) and TNM stage (P = 0.949) between the patients of thyroid malignancies with CLT and without CLT. Female predominance was observed in patients with CLT compared to those without CLT (P < 0.001).

Table 2 The differences in clinicopathological parameters between patients with and without chronic lymphocytic thyroiditis (CLT)
Full size table

Diagnosis results and surgical methods for patients of thyroid malignancies with coexistent chronic lymphocytic thyroiditis

There were 44 patients of thyroid malignancies with coexistent CLT, among which 37 patients had received serological examination. The level of serum thyroperoxidase antibody was elevated in 23 (62.2%) patients, along with the level of thyroglobulin antibodies in 32 (86.5%) patients. Preoperative ultrasonographic examination was applied to the 44 patients who had thyroid malignancies with coexistent CLT: nodular hyperplasia was detected in all patients and accounted for up to 100%, a solitary nodule was found in 15 (34.1%) patients, multiple nodules were present in 19 (65.9%) patients, spot calcification was found in 25 (56.8%) patients, irregular and unclear border appeared in 18 (40.9%) patients, and cervical lymph node enlargement were identified in 23 (52.3%) patients. Seven different surgical methods were assigned to these 44 patients who had thyroid malignancies and co-existing CLT. In total, 13 (29.5%) patients received a unilateral lobectomy plus central region lymph node dissection, and 10 (22.7%) patients received a unilateral lobectomy plus contralateral subtotal lobectomy with central region lymph node dissection. Moreover, a bilateral thyroidectomy plus central region lymph node dissection was assigned to six (13.6%) patients. In addition, 12 (27.3%) patients were equally allotted to 3 groups using bilateral thyroidectomy plus central region lymph node dissection, bilateral thyroidectomy plus unilateral neck dissection and bilateral thyroidectomy plus bilateral neck dissection. The other three (6.8%) patients received unilateral lobectomy plus unilateral neck dissection. All patients received endocrine therapy by means of oral drugs such as levothyroxine sodium, as well as the clinical follow-up after operation. The follow-up period was from 10 months to 22 months (average 15 months). There was no death or case recurrence.

Discussion

The association between CLT and thyroid lymphoma and PTC has been well-established in Japan and America; however, the correlation between CLT and PTC in our country, as well as the influence of CLT on other thyroid malignancies, still needs to be studied. In our study, the association of CLT with clinicopathological parameters of patients with thyroid malignancies was evaluated. The results showed that the morbidity of thyroid malignancies in patients with CLT was significantly higher than that in patients without CLT. A female preponderance was observed in the patients with CLT compared with those without CLT. There was no statistically significant difference in the tumor size, multifocality, neck lymph node metastasis, age, microcarcinoma or TNM stage between the patients of thyroid malignancies with CLT and without CLT.

Among the 44 patients who had thyroid malignancies coexistent with CLT, 41 had been diagnosed with papillary carcinoma, 2 suffered from medullary carcinoma and 1 suffered from lymphoma. The results revealed that coexistence of CLT mainly occurred in the patients with PTC[21, 22], a result in accordance with other studies. In addition, we found that the rate of thyroid malignancies in patients with CLT (40.7%) is significantly higher than that in patients without CLT (18.6%). The presence of CLT has been reported to be in 0.5 to 38% of patients with PTC[17, 18, 23]. The presence of thyroid malignancies in patients with CLT in our study is slightly higher than that reported in the literature. The reasons may be multifactorial. First, the indications for surgery in our department are stricter, and the surgery was performed on patients with thyroid nodules that were highly suspected for thyroid cancer. Second, racial difference, genetic factors, and dietary factors might contribute to the result. Third, it should be note that the sample size of our study was relatively small compared with other studies, consisting of only 647 people. Some studies have reported that the prevalence of CLT is significantly increased in patients with PTC[24, 25]. Therefore, patients with thyroid nodules and who are suspected of having CLT need to be carefully monitored since the possibility of malignancy is raised. Once thyroid cancer is diagnosed, the most cost-effective approach should be chosen. Several treatment methods for patients with thyroid cancer, such as surgical resection, radioactive iodine ablation, and TSH suppression therapy, are all in favor[26]. However, controversy still exists in many areas. Accordingly, thyroidectomy is recommended for differentiated cancer (for example, papillary and follicular cancer)[7]. In contrast, for undifferentiated thyroid cancer (for example, anaplastic cancer) that is associated with aggression and invasion, chemotherapy and radiation treatment might provide more benefit to these patients compared to surgery[27]. In our study, among the 44 patients who had thyroid malignancies and co-existing CLT, papillary carcinoma was the main type of thyroid malignancy. Therefore, seven different surgical methods were assigned to these 44 patients. In addition, endocrine therapy, such as oral drugs, was provided to all patients after operation. Adjuvant therapy was also assigned to patients with extracapsular extensions or more lymph node metastasis. In our subsequent follow-up after operation, we found that there was no case of death or recurrence, possibly due to a good prognosis for thyroid malignancies and the short term of the follow-up.

In our study, a female predominance was observed in patients with CLT compared to those without CLT. Many previous studies have found that patients with CLT are predominately female in comparison with patients without CLT[28, 29]. This result is consistent with previous studies. However, no statistically significant difference was found in the tumor size, multifocality, neck lymph node metastasis, age, microcarcinoma and TNM stage between patients with thyroid malignancies and CLT and those patients with thyroid malignancies and no CLT. Generally speaking, immune infiltration in human tumors as a prognostic factor could not be ignored[30, 31]. CLT is characterized by progressive loss of thyroid epithelial cells and replacement of inflammatory cell infiltrate that produces chemokines, growth factors and cytokines[32–34]. Some studies have reported that the lymphocytic infiltration in PTC is associated with a lower recurrence rate, a better prognosis, and less aggressive disease[19, 35, 36]. However, Kebebew et al. have reported that thyroid lymphocytic infiltration is not an independent prognostic factor and could not reduce the recurrence rate or frequency of distant metastasis[23]. Among the 37 patients who received serological examination, we found that the level of serum thyroperoxidase antibody was high in 23 (62.2%) patients, as well as the level of thyroglobulin antibodies in 32 (86.5%) patients. Because thyroglobulin and thyroperoxidase are the two primary antigens in autoimmune thyroiditis, patients who suffered from CLT would make corresponding autoantibodies against thyroid-specific antigens[32, 37, 38]. It has been reported that serum thyroglobulin antibody was an independent predictor for thyroid malignancy in thyroid nodules[34, 39].

Conclusions

In conclusion, we analyzed the association of CLT with clinicopathological parameters of patients with thyroid malignancies. The results of our study indicate that the CLT may have no effect on the progression of thyroid malignant tumor. Nevertheless, the influences of CLT on the prognosis of the thyroid carcinoma still need to be investigated based on a larger sample size.

Abbreviations

CLT:

chronic lymphocytic thyroiditis

HT:

Hashimoto's thyroiditis

PTC:

papillary thyroid carcinoma

TNM:

tumor–node–metastasis.

References

  1. Brown RL, de Souza JA, Cohen EE: Thyroid cancer: burden of illness and management of disease. J Cancer. 2011, 2: 193-199.

    Article  PubMed Central  PubMed  Google Scholar 

  2. Ahn D, Heo SJ, Park JH, Kim JH, Sohn JH, Park JY, Park SK, Park J: Clinical relationship between Hashimoto's thyroiditis and papillary thyroid cancer. Acta Oncol. 2011, 50: 1228-1234. 10.3109/0284186X.2011.602109.

    Article  PubMed  Google Scholar 

  3. Davies L, Welch HG: Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA. 2006, 295: 2164-2167. 10.1001/jama.295.18.2164.

    Article  CAS  PubMed  Google Scholar 

  4. Koo BS, Yoon YH, Kim JM, Choi EC, Lim YC: Predictive factors of level IIb lymph node metastasis in patients with papillary thyroid carcinoma. Ann Surg Oncol. 2009, 16: 1344-1347. 10.1245/s10434-009-0367-y.

    Article  PubMed  Google Scholar 

  5. Mercante G, Frasoldati A, Pedroni C, Formisano D, Renna L, Piana S, Gardini G, Valcavi R, Barbieri V: Prognostic factors affecting neck lymph node recurrence and distant metastasis in papillary microcarcinoma of the thyroid: results of a study in 445 patients. Thyroid. 2009, 19: 707-716. 10.1089/thy.2008.0270.

    Article  CAS  PubMed  Google Scholar 

  6. Sciuto R, Romano L, Rea S, Marandino F, Sperduti I, Maini CL: Natural history and clinical outcome of differentiated thyroid carcinoma: a retrospective analysis of 1503 patients treated at a single institution. Ann Oncol. 2009, 20: 1728-1735. 10.1093/annonc/mdp050.

    Article  CAS  PubMed  Google Scholar 

  7. Udelsman R, Chen H: The current management of thyroid cancer. Adv Surg. 1999, 33: 1-27.

    CAS  PubMed  Google Scholar 

  8. Mack LA, Pasieka JL: An evidence-based approach to the treatment of thyroid lymphoma. World J Surg. 2007, 31: 978-986. 10.1007/s00268-005-0768-z.

    Article  PubMed  Google Scholar 

  9. Hiromatsu Y, Satoh H, Amino N: Hashimoto's thyroiditis: history and future outlook. Hormones (Athens). 2013, 12: 12-18.

    Google Scholar 

  10. Dailey ME, Lindsay S, Skahen R: Relation of thyroid neoplasms to Hashimoto disease of the thyroid gland. AMA Arch Surg. 1955, 70: 291-297. 10.1001/archsurg.1955.01270080137023.

    Article  CAS  PubMed  Google Scholar 

  11. Dayan CM, Daniels GH: Chronic autoimmune thyroiditis. N Engl J Med. 1996, 335: 99-107. 10.1056/NEJM199607113350206.

    Article  CAS  PubMed  Google Scholar 

  12. Pearce EN, Farwell AP, Braverman LE: Thyroiditis. N Engl J Med. 2003, 348: 2646-2655. 10.1056/NEJMra021194.

    Article  PubMed  Google Scholar 

  13. Holm L-E, Blomgren H, Löwhagen T: Cancer risks in patients with chronic lymphocytic thyroiditis. N Engl J Med. 1985, 312: 601-604. 10.1056/NEJM198503073121001.

    Article  CAS  PubMed  Google Scholar 

  14. Lee JH, Kim Y, Choi JW, Kim YS: The association between papillary thyroid carcinoma and histologically proven Hashimoto's thyroiditis: a meta-analysis. Eur J Endocrinol. 2013, 168: 343-349. 10.1530/EJE-12-0903.

    Article  CAS  PubMed  Google Scholar 

  15. Cipolla C, Sandonato L, Graceffa G, Fricano S, Torcivia A, Vieni S, Latteri S, Latteri MA: Hashimoto thyroiditis coexistent with papillary thyroid carcinoma. Am Surg. 2005, 71: 874-878.

    PubMed  Google Scholar 

  16. Moshynska OV, Saxena A: Clonal relationship between Hashimoto thyroiditis and thyroid lymphoma. J Clin Pathol. 2008, 61: 438-444. 10.1136/jcp.2007.051243.

    Article  CAS  PubMed  Google Scholar 

  17. Okayasu I, Fujiwara M, Hara Y, Tanaka Y, Rose NR: Association of chronic lymphocytic thyroiditis and thyroid papillary carcinoma. A study of surgical cases among Japanese, and white and African Americans. Cancer. 1995, 76: 2312-2318. 10.1002/1097-0142(19951201)76:11<2312::AID-CNCR2820761120>3.0.CO;2-H.

    Article  CAS  PubMed  Google Scholar 

  18. Kim EY, Kim WG, Kim WB, Kim TY, Kim JM, Ryu JS, Hong SJ, Gong G, Shong YK: Coexistence of chronic lymphocytic thyroiditis is associated with lower recurrence rates in patients with papillary thyroid carcinoma. Clin Endocrinol. 2009, 71: 581-586. 10.1111/j.1365-2265.2009.03537.x.

    Article  Google Scholar 

  19. Kashima K, Yokoyama S, Noguchi S, Murakami N, Yamashita H, Watanabe S, Uchino S, Toda M, Sasaki A, Daa T: Chronic thyroiditis as a favorable prognostic factor in papillary thyroid carcinoma. Thyroid. 1998, 8: 197-202. 10.1089/thy.1998.8.197.

    Article  CAS  PubMed  Google Scholar 

  20. Hunt JL, Baloch ZW, Swalsky PA, Trusky CL, Finkelstein S, LiVolsi VA: Loss of heterozygosity mutations to tumor suppressor genes in cytologically atypical areas in chronic lymphocytic thyroiditis. Endocr Pathol. 2002, 13: 321-329. 10.1385/EP:13:4:321.

    Article  CAS  PubMed  Google Scholar 

  21. Diklić A, Zivaljević V, Paunović I, Kalezić N, Tatić S: Surgical procedures in patients with thyroid autoimmune disease. Srp Arh Celok Lek. 2005, 133: 77-83.

    Article  PubMed  Google Scholar 

  22. Shih M-L, Lee JA, Hsieh C-B, Yu J-C, Liu H-D, Kebebew E, Clark OH, Duh Q-Y: Thyroidectomy for Hashimoto's thyroiditis: complications and associated cancers. Thyroid. 2008, 18: 729-734. 10.1089/thy.2007.0384.

    Article  PubMed  Google Scholar 

  23. Kebebew E, Treseler PA, Ituarte PH, Clark OH: Coexisting chronic lymphocytic thyroiditis and papillary thyroid cancer revisited. World J Surg. 2001, 25: 632-637. 10.1007/s002680020165.

    Article  CAS  PubMed  Google Scholar 

  24. Singh B, Shaha AR, Trivedi H, Carew JF, Poluri A, Shah JP: Coexistent Hashimoto's thyroiditis with papillary thyroid carcinoma: impact on presentation, management, and outcome. Surgery. 1999, 126: 1070-1077. 10.1067/msy.2099.101431.

    Article  CAS  PubMed  Google Scholar 

  25. Repplinger D, Bargren A, Zhang Y-W, Adler JT, Haymart M, Chen H: Is Hashimoto's thyroiditis a risk factor for papillary thyroid cancer?. J Surg Res. 2008, 150: 49-52. 10.1016/j.jss.2007.09.020.

    Article  PubMed Central  PubMed  Google Scholar 

  26. Zarebczan B, Chen H: Multi-targeted approach in the treatment of thyroid cancer. Minerva Chir. 2010, 65: 59-69.

    PubMed Central  CAS  PubMed  Google Scholar 

  27. Haugen BR: Management of the patient with progressive radioiodine non-responsive disease. Semin Surg Oncol. 1999, 16: 34-41. 10.1002/(SICI)1098-2388(199901/02)16:1<34::AID-SSU7>3.0.CO;2-2.

    Article  CAS  PubMed  Google Scholar 

  28. Yoon Y-H, Kim HJ, Lee JW, Kim JM, Koo BS: The clinicopathologic differences in papillary thyroid carcinoma with or without co-existing chronic lymphocytic thyroiditis. Eur Arch Otorhinolaryngol. 2012, 269: 1013-1017. 10.1007/s00405-011-1732-6.

    Article  PubMed  Google Scholar 

  29. Jeong JS, Kim HK, Lee C-R, Park S, Park JH, Kang S-W, Jeong JJ, Nam K-H, Chung WY, Park CS: Coexistence of chronic lymphocytic thyroiditis with papillary thyroid carcinoma: clinical manifestation and prognostic outcome. J Korean Med Sci. 2012, 27: 883-889. 10.3346/jkms.2012.27.8.883.

    Article  PubMed Central  PubMed  Google Scholar 

  30. Pages F, Galon J, Dieu-Nosjean M, Tartour E, Sautes-Fridman C, Fridman W: Immune infiltration in human tumors: a prognostic factor that should not be ignored. Oncogene. 2010, 29: 1093-1102. 10.1038/onc.2009.416.

    Article  CAS  PubMed  Google Scholar 

  31. Mahmoud S, Lee A, Paish E, Macmillan R, Ellis I, Green A: The prognostic significance of B lymphocytes in invasive carcinoma of the breast. Breast Cancer Res Treat. 2012, 132: 545-553. 10.1007/s10549-011-1620-1.

    Article  CAS  PubMed  Google Scholar 

  32. Tomer Y, Menconi F: Interferon induced thyroiditis. Best Pract Res Clin Endocrinol Metab. 2009, 23: 703-712. 10.1016/j.beem.2009.07.004.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Pacifico F, Leonardi A: Role of NF-κB in thyroid cancer. Mol Cell Endocrinol. 2010, 321: 29-35. 10.1016/j.mce.2009.10.010.

    Article  CAS  PubMed  Google Scholar 

  34. Kim ES, Lim DJ, Baek KH, Lee JM, Kim MK, Kwon HS, Song KH, Kang MI, Cha BY, Lee KW: Thyroglobulin antibody is associated with increased cancer risk in thyroid nodules. Thyroid. 2010, 20: 885-891. 10.1089/thy.2009.0384.

    Article  CAS  PubMed  Google Scholar 

  35. Loh K-C, Greenspan FS, Dong F, Miller TR, Yeo PP: Influence of lymphocytic thyroiditis on the prognostic outcome of patients with papillary thyroid carcinoma. J Clin Endocrinol Metab. 1999, 84: 458-463. 10.1210/jcem.84.2.5443.

    Article  CAS  PubMed  Google Scholar 

  36. Meier DW, Woolner LB, Beahrs OH, Mc CW: Parenchymal findings in thyroidal carcinoma: pathologic study of 256 cases. J Clin Endocrinol Metab. 1959, 19: 162-171. 10.1210/jcem-19-1-162.

    Article  CAS  PubMed  Google Scholar 

  37. Burek CL, Rose NR: Autoimmune thyroiditis and ROS. Autoimmun Rev. 2008, 7: 530-537. 10.1016/j.autrev.2008.04.006.

    Article  CAS  PubMed  Google Scholar 

  38. Flynn JC, McCormick DJ, Brusic V, Wan Q, Panos JC, Giraldo AA, David CS, Kong YCM: Pathogenic human thyroglobulin peptides in HLA-DR3 transgenic mouse model of autoimmune thyroiditis. Cell Immunol. 2004, 229: 79-85. 10.1016/j.cellimm.2004.07.002.

    Article  CAS  PubMed  Google Scholar 

  39. Spencer CA: Clinical utility of thyroglobulin antibody (TgAb) measurements for patients with differentiated thyroid cancers (DTC). J Clin Endocrinol Metab. 2011, 96: 3615-3627. 10.1210/jc.2011-1740.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

None.

Author information

Author notes

    Authors and Affiliations

    1. Department of General Surgery, The Affiliated Provincial Hospital of Anhui Medical University, No.1, Tian’ehu Road, 230001, Hefei, China

      Yi Zhang, Xiao-peng Ma, Fu-sheng Deng, Zheng-rong Liu, Hou-qing Wei, Xi-hong Wang & Hao Chen

    Authors
    1. Yi Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Xiao-peng Ma
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Fu-sheng Deng
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Zheng-rong Liu
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Hou-qing Wei
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Xi-hong Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Hao Chen
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Yi Zhang.

    Additional information

    Competing interests

    The authors declare that no competing interests exist.

    Authors’ contributions

    YZ and XM participated in the design of this study, and they both performed the statistical analysis. FD and HC carried out the study together with ZL, collected important background information and drafted the manuscript. HW and XW conceived of this study, participated in the design and helped to draft the manuscript. All authors read and approved the final manuscript.

    Yi Zhang, Xiao-peng Ma contributed equally to this work.

    Rights and permissions

    This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Zhang, Y., Ma, Xp., Deng, Fs. et al. The effect of chronic lymphocytic thyroiditis on patients with thyroid cancer. World J Surg Onc 12, 277 (2014). https://doi.org/10.1186/1477-7819-12-277

    Download citation

    • Received:

    • Accepted:

    • Published:

    • DOI: https://doi.org/10.1186/1477-7819-12-277

    Keywords

    World Journal of Surgical Oncology

    ISSN: 1477-7819

    Contact us