Skip to main content

Advertisement

SpringerLink
Log in

Dysbiosis of the gut microbiome is associated with thyroid cancer and thyroid nodules and correlated with clinical index of thyroid function

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Purpose

Thyroid cancer and thyroid nodules are the most prevalent form of thyroid endocrine disorder. The balance of gut microbiome is highly crucial for a healthy human body, especially for the immune and endocrine system. However, the relationship between gut microbiome and the thyroid endocrine disorders such as thyroid cancer and thyroid nodules has not been reported yet.

Methods

A cohort of 74 patients was recruited for this study. Among them, 20 patients had thyroid cancer, 18 patients had thyroid nodules, and 36 were matched healthy controls. Gut microbiome composition was analyzed by 16S rRNA (16S ribosomal RNA) gene-based sequencing protocol.

Results

We compared the gut microbiome results of 74 subjects and established the correlation between gut microbiome and thyroid endocrine function for both thyroid cancer and thyroid nodules. The results inferred that alpha and beta diversity were different for patients with thyroid tumor than the healthy controls (p < 0.01). In comparison to healthy controls, the relative abundance of Neisseria (p < 0.001) and Streptococcus (p < 0.001) was significantly higher for thyroid cancer and thyroid nodules. Butyricimonas (p < 0.001) and Lactobacillus (p < 0.001) displayed notably lower relative abundance for thyroid cancer and thyroid nodules, respectively. It was also found that the clinical indexes were correlated with gut microbiome.

Conclusion

Our results indicate that both thyroid cancer and thyroid nodules are associated with the composition of gut microbiome. These results may support further clinical diagnosis to a great extent and help in developing potential probiotics to facilitate the treatment of thyroid cancer and thyroid nodules.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

Tg:

Thyroglobulin

TgAb:

Thyroglobulin antibody

TSH:

Thyroid stimulating hormone

FT3:

Free triiodothyronine

FT4:

Free tetraiodothyronine

TRAb:

Thyrotropin receptor antibody

TPOAb:

Thyroid peroxidase antibody

References

  1. J.A. Gilbert, M.J. Blaser, J.G. Caporaso, J.K. Jansson, S.V. Lynch, R. Knight, Current understanding of the human microbiome. Nat. Med. 24(4), 392–400 (2018). https://doi.org/10.1038/nm.4517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. C. De Filippo, D. Cavalieri, M. Di Paola, M. Ramazzotti, J.B. Poullet, S. Massart, S. Collini, G. Pieraccini, P. Lionetti. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl Acad. Sci. USA. 107(33), 14691-14696 (2010). https://doi.org/10.1073/pnas.1005963107

  3. L. Dethlefsen, M. McFall-Ngai, D.A. Relman, An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449(7164), 811–818 (2007). https://doi.org/10.1038/nature06245

    Article  CAS  PubMed  Google Scholar 

  4. O. Huck, J. Al-Hashemi, L. Poidevin, O. Poch, J.L. Davideau, H. Tenenbaum, S. Amar. identification and characterization of microrna differentially expressed in macrophages exposed to porphyromonas gingivalis infection. Infect. Immunity 85(3), (2017). https://doi.org/10.1128/IAI.00771-16

  5. C. Pere-Vedrenne, M. Prochazkova-Carlotti, B. Rousseau, W. He, L. Chambonnier, E. Sifre, A. Buissonniere, P. Dubus, F. Megraud, C. Varon, A. Menard, The cytolethal distending toxin subunit cdtb of helicobacter hepaticus promotes senescence and endoreplication in xenograft mouse models of hepatic and intestinal cell lines. Front. Cell. Infect. Microbiol. 7, 268 (2017). https://doi.org/10.3389/fcimb.2017.00268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. L. Zitvogel, M. Ayyoub, B. Routy, G. Kroemer, Microbiome and anticancer immunosurveillance. Cell 165(2), 276–287 (2016). https://doi.org/10.1016/j.cell.2016.03.001

    Article  CAS  PubMed  Google Scholar 

  7. Y. Guo, Y. Qi, X. Yang, L. Zhao, S. Wen, Y. Liu, L. Tang, Association between Polycystic Ovary Syndrome and Gut Microbiota. PloS One 11(4), e0153196 (2016). https://doi.org/10.1371/journal.pone.0153196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. R.J. Perry, L. Peng, N.A. Barry, G.W. Cline, D. Zhang, R.L. Cardone, K.F. Petersen, R.G. Kibbey, A.L. Goodman, G.I. Shulman, Acetate mediates a microbiome-brain-beta-cell axis to promote metabolic syndrome. Nature 534(7606), 213–217 (2016). https://doi.org/10.1038/nature18309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. T. Vatanen, E.A. Franzosa, R. Schwager, S. Tripathi, T.D. Arthur, K. Vehik, A. Lernmark, W.A. Hagopian, M.J. Rewers, J.X. She, J. Toppari, A.G. Ziegler, B. Akolkar, J.P. Krischer, C.J. Stewart, N.J. Ajami, J.F. Petrosino, D. Gevers, H. Lahdesmaki, H. Vlamakis, C. Huttenhower, R.J. Xavier, The human gut microbiome in early-onset type 1 diabetes from the TEDDY study. Nature 562(7728), 589–594 (2018). https://doi.org/10.1038/s41586-018-0620-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. K. Forslund, F. Hildebrand, T. Nielsen, G. Falony, E. Le Chatelier, S. Sunagawa, E. Prifti, S. Vieira-Silva, V. Gudmundsdottir, H.K. Pedersen, M. Arumugam, K. Kristiansen, A.Y. Voigt, H. Vestergaard, R. Hercog, P.I. Costea, J.R. Kultima, J. Li, T. Jorgensen, F. Levenez, J. Dore, H.I.Tc Meta, H.B. Nielsen, S. Brunak, J. Raes, T. Hansen, J. Wang, S.D. Ehrlich, P. Bork, O. Pedersen, Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 528(7581), 262–266 (2015). https://doi.org/10.1038/nature15766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. C.F.L. Goncalves, M.L. de Freitas, A.C.F. Ferreira. Flavonoids, thyroid iodide uptake and thyroid cancer-a review. Int. J. Mol. Sci. 18(6), (2017). https://doi.org/10.3390/ijms18061247

  12. T. Carling, R. Udelsman, Thyroid cancer. Annu. Rev. Med. 65, 125–137 (2014). https://doi.org/10.1146/annurev-med-061512-105739

    Article  CAS  PubMed  Google Scholar 

  13. J. Ferlay, I. Soerjomataram, R. Dikshit, S. Eser, C. Mathers, M. Rebelo, D.M. Parkin, D. Forman, F. Bray, Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer 136(5), E359–386 (2015). https://doi.org/10.1002/ijc.29210

    Article  CAS  PubMed  Google Scholar 

  14. G. Pellegriti, F. Frasca, C. Regalbuto, S. Squatrito, R. Vigneri, Worldwide increasing incidence of thyroid cancer: update on epidemiology and risk factors. J. Cancer Epidemiol. 2013, 965212 (2013). https://doi.org/10.1155/2013/965212

    Article  PubMed  PubMed Central  Google Scholar 

  15. L. Rahib, B.D. Smith, R. Aizenberg, A.B. Rosenzweig, J.M. Fleshman, L.M. Matrisian, Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res. 74(11), 2913–2921 (2014). https://doi.org/10.1158/0008-5472.CAN-14-0155

    Article  CAS  PubMed  Google Scholar 

  16. D.M. Parkin, J. Ferlay, M.P. Curado, F. Bray, B. Edwards, H.R. Shin, D. Forman, Fifty years of cancer incidence: CI5 I-IX. Int. J. Cancer 127(12), 2918–2927 (2010). https://doi.org/10.1002/ijc.25517

    Article  CAS  PubMed  Google Scholar 

  17. K.D. Burman, L. Wartofsky, Clinical practice. thyroid nodules. New Engl. J. Med. 373(24), 2347–2356 (2015). https://doi.org/10.1056/NEJMcp1415786

    Article  CAS  PubMed  Google Scholar 

  18. S. Guth, U. Theune, J. Aberle, A. Galach, C.M. Bamberger, Very high prevalence of thyroid nodules detected by high frequency (13 MHz) ultrasound examination. Eur. J. Clin. Investig. 39(8), 699–706 (2009). https://doi.org/10.1111/j.1365-2362.2009.02162.x

    Article  CAS  Google Scholar 

  19. F. Clavel-Chapelon, G. Guillas, L. Tondeur, C. Kernaleguen, M.C. Boutron-Ruault, Risk of differentiated thyroid cancer in relation to adult weight, height and body shape over life: the French E3N cohort. Int. J. Cancer 126(12), 2984–2990 (2010). https://doi.org/10.1002/ijc.25066

    Article  CAS  PubMed  Google Scholar 

  20. A. Magreni, D.V. Bann, J.R. Schubart, D. Goldenberg, The effects of race and ethnicity on thyroid cancer incidence. JAMA Otolaryngol. Head. Neck Surg. 141(4), 319–323 (2015). https://doi.org/10.1001/jamaoto.2014.3740

    Article  PubMed  Google Scholar 

  21. M. Sokouti, V. Montazeri, A. Fakhrjou, S. Samankan, M. Goldust, Thyroid cancer, clinical and hystopathological study on patients under 25 years in Tabriz, Iran (2000-2012). Pak. J. Biol. Sci.: PJBS 16(24), 2003–2008 (2013)

    Article  PubMed  Google Scholar 

  22. L.H. Veiga, E. Holmberg, H. Anderson, L. Pottern, S. Sadetzki, M.J. Adams, R. Sakata, A.B. Schneider, P. Inskip, P. Bhatti, R. Johansson, G. Neta, R. Shore, F. de Vathaire, L. Damber, R. Kleinerman, M.M. Hawkins, M. Tucker, M. Lundell, J.H. Lubin, Thyroid cancer after childhood exposure to external radiation: an updated pooled analysis of 12 studies. Radiat. Res. 185(5), 473–484 (2016). https://doi.org/10.1667/RR14213.1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. M. Zane, C. Parello, G. Pennelli, D.M. Townsend, S. Merigliano, M. Boscaro, A. Toniato, G. Baggio, M.R. Pelizzo, D. Rubello, I.M. Boschin, Estrogen and thyroid cancer is a stem affair: a preliminary study. Biomed. Pharmacother. 85, 399–411 (2017). https://doi.org/10.1016/j.biopha.2016.11.043

    Article  CAS  PubMed  Google Scholar 

  24. C. Virili, M. Centanni, “With a little help from my friends” - The role of microbiota in thyroid hormone metabolism and enterohepatic recycling. Mol. Cell. Endocrinol. 458, 39–43 (2017). https://doi.org/10.1016/j.mce.2017.01.053

    Article  CAS  PubMed  Google Scholar 

  25. E. Jasarevic, K.E. Morrison, T.L. Bale, Sex differences in the gut microbiome-brain axis across the lifespan. Philosophical transactions of the Royal Society of London. Ser. B, Biol. Sci. 371(1688), 20150122 (2016). https://doi.org/10.1098/rstb.2015.0122

    Article  CAS  Google Scholar 

  26. D. Covelli, M. Ludgate, The thyroid, the eyes and the gut: a possible connection. J. Endocrinol. Investig. 40(6), 567–576 (2017). https://doi.org/10.1007/s40618-016-0594-6

    Article  CAS  Google Scholar 

  27. H.M. Ishaq, I.S. Mohammad, H. Guo, M. Shahzad, Y.J. Hou, C. Ma, Z. Naseem, X. Wu, P. Shi, J. Xu, Molecular estimation of alteration in intestinal microbial composition in Hashimoto’s thyroiditis patients. Biomed. Pharmacother. 95, 865–874 (2017). https://doi.org/10.1016/j.biopha.2017.08.101

    Article  CAS  PubMed  Google Scholar 

  28. F. Zhao, J. Feng, J. Li, L. Zhao, Y. Liu, H. Chen, Y. Jin, B. Zhu, Y. Wei, Alterations of the gut microbiota in hashimoto’s thyroiditis patients. Thyroid 28(2), 175–186 (2018). https://doi.org/10.1089/thy.2017.0395

    Article  CAS  PubMed  Google Scholar 

  29. X. Wang, L. Zhang, Y. Wang, X. Liu, H. Zhang, Y. Liu, N. Shen, J. Yang, Z. Gai, Gut microbiota dysbiosis is associated with Henoch-Schonlein Purpura in children. Int. Immunopharmacol. 58, 1–8 (2018). https://doi.org/10.1016/j.intimp.2018.03.003

    Article  CAS  PubMed  Google Scholar 

  30. K. Findley, J. Oh, J. Yang, S. Conlan, C. Deming, J.A. Meyer, D. Schoenfeld, E. Nomicos, M. Park; Program, N.I.H.I.S.C.C.S., H.H. Kong, J.A. Segre, Topographic diversity of fungal and bacterial communities in human skin. Nature 498(7454), 367–370 (2013). https://doi.org/10.1038/nature12171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. T. Magoc, S.L. Salzberg, FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21), 2957–2963 (2011). https://doi.org/10.1093/bioinformatics/btr507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. J.G. Caporaso, J. Kuczynski, J. Stombaugh, K. Bittinger, F.D. Bushman, E.K. Costello, N. Fierer, A.G. Pena, J.K. Goodrich, J.I. Gordon, G.A. Huttley, S.T. Kelley, D. Knights, J.E. Koenig, R.E. Ley, C.A. Lozupone, D. McDonald, B.D. Muegge, M. Pirrung, J. Reeder, J.R. Sevinsky, P.J. Turnbaugh, W.A. Walters, J. Widmann, T. Yatsunenko, J. Zaneveld, R. Knight, QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7(5), 335–336 (2010). https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. R.C. Edgar, Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19), 2460 (2010)

    Article  CAS  PubMed  Google Scholar 

  34. J.R. Cole, Q. Wang, E. Cardenas, J. Fish, B. Chai, R.J. Farris, A.S. Kulam-Syed-Mohideen, D.M. McGarrell, T. Marsh, G.M. Garrity, J.M. Tiedje, The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37(Database issue), D141–145 (2009). https://doi.org/10.1093/nar/gkn879

    Article  CAS  PubMed  Google Scholar 

  35. S.V. Rajagopala, S. Vashee, L.M. Oldfield, Y. Suzuki, J.C. Venter, A. Telenti, K.E. Nelson, The human microbiome and cancer. Cancer Prev. Res. 10(4), 226–234 (2017). https://doi.org/10.1158/1940-6207.CAPR-16-0249

    Article  Google Scholar 

  36. S. Meng, B. Chen, J. Yang, J. Wang, D. Zhu, Q. Meng, L. Zhang, Study of microbiomes in aseptically collected samples of human breast tissue using needle biopsy and the potential role of in situ tissue microbiomes for promoting malignancy. Front Oncol. 8, 318 (2018). https://doi.org/10.3389/fonc.2018.00318

    Article  PubMed  PubMed Central  Google Scholar 

  37. X. Wang, T. Ye, W.J. Chen, Y. Lv, Z. Hao, J. Chen, J.Y. Zhao, H.P. Wang, Y.K. Cai, Structural shift of gut microbiota during chemo-preventive effects of epigallocatechin gallate on colorectal carcinogenesis in mice. World J. Gastroenterol. 23(46), 8128–8139 (2017). https://doi.org/10.3748/wjg.v23.i46.8128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. J. Zhu, M. Liao, Z. Yao, W. Liang, Q. Li, J. Liu, H. Yang, Y. Ji, W. Wei, A. Tan, S. Liang, Y. Chen, H. Lin, X. Zhu, S. Huang, J. Tian, R. Tang, Q. Wang, Z. Mo, Breast cancer in postmenopausal women is associated with an altered gut metagenome. Microbiome 6(1), 136 (2018). https://doi.org/10.1186/s40168-018-0515-3

    Article  PubMed  PubMed Central  Google Scholar 

  39. K.M. Trapani, L.J. Boghossian, E. Caskey, Clostridium subterminale Septicemia in a patient with metastatic gastrointestinal adenocarcinoma. Case Rep. Infect. Dis. 2018, 6031510 (2018). https://doi.org/10.1155/2018/6031510

    Article  PubMed  PubMed Central  Google Scholar 

  40. A.J. Benitez, C. Hoffmann, A.B. Muir, K.K. Dods, J.M. Spergel, F.D. Bushman, M.L. Wang, Inflammation-associated microbiota in pediatric eosinophilic esophagitis. Microbiome 3, 23 (2015). https://doi.org/10.1186/s40168-015-0085-6

    Article  PubMed  PubMed Central  Google Scholar 

  41. S. Macfarlane, E. Furrie, G.T. Macfarlane, J.F. Dillon, Microbial colonization of the upper gastrointestinal tract in patients with Barrett’s esophagus. Clin. Infect. Dis. 45(1), 29–38 (2007). https://doi.org/10.1086/518578

    Article  PubMed  Google Scholar 

  42. J. Si, C. Lee, G. Ko, Oral microbiota: microbial biomarkers of metabolic syndrome independent of host genetic factors. Front Cell Infect. Microbiol 7, 516 (2017). https://doi.org/10.3389/fcimb.2017.00516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. R. Memba, S.N. Duggan, H.M. Ni Chonchubhair, O.M. Griffin, Y. Bashir, D.B. O’Connor, A. Murphy, J. McMahon, Y. Volcov, B.M. Ryan, K.C. Conlon, The potential role of gut microbiota in pancreatic disease: a systematic review. Pancreatology 17(6), 867–874 (2017). https://doi.org/10.1016/j.pan.2017.09.002

    Article  CAS  PubMed  Google Scholar 

  44. J.S. Gold, S. Bayar, R.R. Salem, Association of Streptococcus bovis bacteremia with colonic neoplasia and extracolonic malignancy. Arch. Surg. 139(7), 760–765 (2004). https://doi.org/10.1001/archsurg.139.7.760

    Article  PubMed  Google Scholar 

  45. A.S. Abdulamir, R.R. Hafidh, F. Abu Bakar, The association of Streptococcus bovis/gallolyticus with colorectal tumors: the nature and the underlying mechanisms of its etiological role. J. Exp. Clin. Cancer Res 30, 11 (2011). https://doi.org/10.1186/1756-9966-30-11

    Article  PubMed  PubMed Central  Google Scholar 

  46. J.D. Dahmus, D.L. Kotler, D.M. Kastenberg, C.A. Kistler, The gut microbiome and colorectal cancer: a review of bacterial pathogenesis. J. Gastrointest. Oncol. 9(4), 769–777 (2018). https://doi.org/10.21037/jgo.2018.04.07

    Article  PubMed  PubMed Central  Google Scholar 

  47. M. Sakamoto, A. Takagaki, K. Matsumoto, Y. Kato, K. Goto, Y. Benno, Butyricimonas synergistica gen. nov., sp. nov. and Butyricimonas virosa sp. nov., butyric acid-producing bacteria in the family ‘Porphyromonadaceae’ isolated from rat faeces. Int. J. Syst. Evolut. Microbiol. 59(Pt 7), 1748–1753 (2009). https://doi.org/10.1099/ijs.0.007674-0

    Article  CAS  Google Scholar 

  48. J. Zhao, L. Nian, L.Y. Kwok, T. Sun, J. Zhao, Reduction in fecal microbiota diversity and short-chain fatty acid producers in Methicillin-resistant Staphylococcus aureus infected individuals as revealed by PacBio single molecule, real-time sequencing technology. Eur. J. Clin. Microbiol. Infect. Dis. 36(8), 1463–1472 (2017). https://doi.org/10.1007/s10096-017-2955-2

    Article  CAS  PubMed  Google Scholar 

  49. Y. Furusawa, Y. Obata, S. Fukuda, T.A. Endo, G. Nakato, D. Takahashi, Y. Nakanishi, C. Uetake, K. Kato, T. Kato, M. Takahashi, N.N. Fukuda, S. Murakami, E. Miyauchi, S. Hino, K. Atarashi, S. Onawa, Y. Fujimura, T. Lockett, J.M. Clarke, D.L. Topping, M. Tomita, S. Hori, O. Ohara, T. Morita, H. Koseki, J. Kikuchi, K. Honda, K. Hase, H. Ohno, Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504(7480), 446–450 (2013). https://doi.org/10.1038/nature12721

    Article  CAS  PubMed  Google Scholar 

  50. E. Pessione, Lactic acid bacteria contribution to gut microbiota complexity: lights and shadows. Front. Cell. Infect. Microbiol. 2, 86 (2012). https://doi.org/10.3389/fcimb.2012.00086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. S. Danzi, I. Klein, Thyroid hormone and the cardiovascular system. Med. Clin. North Am. 96(2), 257–268 (2012). https://doi.org/10.1016/j.mcna.2012.01.006

    Article  CAS  PubMed  Google Scholar 

  52. A.P. Garcia-Gonzalez, A.D. Ritter, S. Shrestha, E.C. Andersen, L.S. Yilmaz, A.J.M. Walhout, Bacterial metabolism affects the C. elegans response to cancer chemotherapeutics. Cell 169(3), 431–441 e438 (2017). https://doi.org/10.1016/j.cell.2017.03.046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. V. Gopalakrishnan, C.N. Spencer, L. Nezi, A. Reuben, M.C. Andrews, T.V. Karpinets, P.A. Prieto, D. Vicente, K. Hoffman, S.C. Wei, A.P. Cogdill, L. Zhao, C.W. Hudgens, D.S. Hutchinson, T. Manzo, M. Petaccia de Macedo, T. Cotechini, T. Kumar, W.S. Chen, S.M. Reddy, R. Szczepaniak Sloane, J. Galloway-Pena, H. Jiang, P.L. Chen, E.J. Shpall, K. Rezvani, A.M. Alousi, R.F. Chemaly, S. Shelburne, L.M. Vence, P.C. Okhuysen, V.B. Jensen, A.G. Swennes, F. McAllister, E. Marcelo Riquelme Sanchez, Y. Zhang, E. Le Chatelier, L. Zitvogel, N. Pons, J.L. Austin-Breneman, L.E. Haydu, E.M. Burton, J.M. Gardner, E. Sirmans, J. Hu, A.J. Lazar, T. Tsujikawa, A. Diab, H. Tawbi, I.C. Glitza, W.J. Hwu, S.P. Patel, S.E. Woodman, R.N. Amaria, M.A. Davies, J.E. Gershenwald, P. Hwu, J.E. Lee, J. Zhang, L.M. Coussens, Z.A. Cooper, P.A. Futreal, C.R. Daniel, N.J. Ajami, J.F. Petrosino, M.T. Tetzlaff, P. Sharma, J.P. Allison, R.R. Jenq, J.A. Wargo, Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 359(6371), 97–103 (2018). https://doi.org/10.1126/science.aan4236

    Article  CAS  PubMed  Google Scholar 

  54. Y. Gu, X. Wang, J. Li, Y. Zhang, H. Zhong, R. Liu, D. Zhang, Q. Feng, X. Xie, J. Hong, H. Ren, W. Liu, J. Ma, Q. Su, H. Zhang, J. Yang, X. Wang, X. Zhao, W. Gu, Y. Bi, Y. Peng, X. Xu, H. Xia, F. Li, X. Xu, H. Yang, G. Xu, L. Madsen, K. Kristiansen, G. Ning, W. Wang, Analyses of gut microbiota and plasma bile acids enable stratification of patients for antidiabetic treatment. Nat. Commun. 8(1), 1785 (2017). https://doi.org/10.1038/s41467-017-01682-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. H. Zhao, H. Li, T. Huang, High urinary iodine, thyroid autoantibodies, and thyroid-stimulating hormone for papillary thyroid cancer risk. Biol. Trace Elem. Res. 184(2), 317–324 (2018). https://doi.org/10.1007/s12011-017-1209-6

    Article  CAS  PubMed  Google Scholar 

  56. R. Guerrero-Preston, F. Godoy-Vitorino, A. Jedlicka, A. Rodriguez-Hilario, H. Gonzalez, J. Bondy, F. Lawson, O. Folawiyo, C. Michailidi, A. Dziedzic, R. Thangavel, T. Hadar, M.G. Noordhuis, W. Westra, W. Koch, D. Sidransky, 16S rRNA amplicon sequencing identifies microbiota associated with oral cancer, human papilloma virus infection and surgical treatment. Oncotarget 7(32), 51320–51334 (2016). https://doi.org/10.18632/oncotarget.9710

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was supported by the National Natural Science Foundation of China under contract No.31471202 (Lei Zhang) and No. 81670822 (Ye Wang); the Shandong Provincial Key Research and Development Program under contract No. 2016YYSP009 (Lei Zhang); Weihai Technique Extension Project under contract No. 2016GNS023 (Lei Zhang). Qingdao Key Research Project No. 17-3-3-10-nsh (Chunling Zhang). Lei Zhang was also supported by the Taishan Scholars Program of Shandong Province (No. tshw20120206).

Author Contributions

L.Z., J.Y. and M.Y. designed the study. J.Z., C.L., Y.Y., H.W., Y.S., Y.W., X.M., D.Z., and C.Z. performed measurements and data analysis. C.Z. and Q.X. obtained samples. F.Z., J.Z. and L.Z. wrote the manuscript. All authors have read and critically revised the manuscript.

Author information

Author notes

  1. These authors contributed equally: Jiaming Zhang, Fanghua Zhang, Changying Zhao.

  2. Lei Zhang is the lead corresponding author.

Authors and Affiliations

  1. Qingdao Human Microbiome Center, The Affiliated Central Hospital of Qingdao University, Shandong Province, Qingdao, 266042, China

    Jiaming Zhang, Fanghua Zhang, Changying Zhao, Chunling Zhang, Junjie Yang, Minxiu Yao & Lei Zhang

  2. College of Life Science, Shandong Normal University, Shandong Province, Jinan, 250014, China

    Jiaming Zhang & Changying Zhao

  3. Department of Endocrinology, The Affiliated Central Hospital of Qingdao University, Shandong Province, Qingdao, 266042, China

    Fanghua Zhang, Qian Xu, Ying Yang, Huiling Wang, Yongfang Shang, Ye Wang, Xiaofeng Mu & Minxiu Yao

  4. School of Information Science and Engineering, Shandong Normal University, Shandong Province, Jinan, 250014, China

    Cheng Liang

  5. Clinical Laboratory and Core Research Laboratory, The Affiliated Central Hospital of Qingdao University, Shandong Province, Qingdao 266042, China

    Ye Wang & Xiaofeng Mu

  6. Microbiological Laboratory, Lin Yi People’s Hospital, Shandong Province, Linyi 276003, China

    Dequan Zhu & Lei Zhang

  7. College of Life Science, Qilu Normal University, Shandong Province, Jinan, 250200, China

    Junjie Yang

  8. Shandong Children’s Microbiome Center, Qilu Children’s Hospital of Shandong University, Jinan, 250022, China

    Lei Zhang

  9. Shandong Institutes for Food and Drug Control, Xinluo Street 2749, Jinan, Shandong Province, 250101, China

    Lei Zhang

  10. Beijing Advanced Innovation Center for Big Data-Based Precision Medicine, School of Chemistry and Environment, Beihang University, Beijing, 100191, China

    Lei Zhang

Authors
  1. Jiaming Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fanghua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Changying Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qian Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cheng Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ying Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Huiling Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yongfang Shang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ye Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Xiaofeng Mu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Dequan Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Chunling Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Junjie Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Minxiu Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Lei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Junjie Yang, Minxiu Yao or Lei Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest. The authors have nothing to disclose.

Ethical approval

All procedures performed in the above studies involving human participants were in accordance with the ethical standards of the institution and/or national research committee and with the 1964 Declaration of Helsinki along with its later amendments or comparable ethical standards.

Informed consent

All the subjects signed informed consent beforehand and belonged to the same geographical area. Data was collected by using a standardized questionnaire including basic information, medical history and examination results.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, J., Zhang, F., Zhao, C. et al. Dysbiosis of the gut microbiome is associated with thyroid cancer and thyroid nodules and correlated with clinical index of thyroid function. Endocrine 64, 564–574 (2019). https://doi.org/10.1007/s12020-018-1831-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-018-1831-x

Keywords

Search

Navigation