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Interaction effect of obesity and thyroid autoimmunity on the prevalence of hyperthyrotropinaemia

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Abstract

Purpose

The role of thyroid autoimmunity in the association between obesity and hyperthyrotropinaemia remains unclear. We aimed to assess the relationship between obesity, autoimmunity, and hyperthyrotropinaemia.

Methods

In this population-based cross-sectional study, 12531 Chinese individuals (18–80 years) with thyroid function test were categorized into three groups by body mass index (BMI) and were categorized into three layers by thyroid autoantibodies. Multivariate logistic regression was employed to assess the correlation and interaction effect.

Results

There was no significant difference in prevalence of hyperthyrotropinaemia (P = 0.637) among three BMI groups. After stratification, the difference of serum thyrotropin (P < 0.01) and prevalence of hyperthyrotropinaemia (P < 0.01) between the three groups have significant linear trends at the positive levels of thyroid peroxidase antibody (TPOAb) or/and thyroglobulin antibody (TgAb). When TPOAb and TgAb were positive, the risk of hyperthyrotropinaemia increased 1.857-fold in overweight group and 2.201-fold in obese group compared with normal group. Compared with negative TPOAb and TgAb, the risk of hyperthyrotropinaemia for individuals with two positive antibodies increased 3.310-fold, 4.969-fold, and 5.122-fold in the three BMI groups. The adjusted OR (95% CI) for interaction were 1.033 (0.752–1.419) for overweight and one positive antibodies, 1.935 (1.252–2.990) for overweight and two positive antibodies, 1.435 (0.978–2.105) for obesity and one positive antibodies and 2.191 (1.252–3.832) for obesity and two positive antibodies.

Conclusion

Overweight and obesity were associated with hyperthyrotropinaemia only in presence of thyroid autoimmunity, and obesity might aggravate the pathogenic effect of autoimmunity on hyperthyrotropinaemia. There was an interaction effect between obesity and autoimmunity on the prevalence of hyperthyrotropinaemia.

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References

  1. G.B.D.O. Collaborators, A. Afshin, M.H. Forouzanfar, M.B. Reitsma, P. Sur, K. Estep, A. Lee, L. Marczak, A.H. Mokdad, M. Moradi-Lakeh, M. Naghavi, J.S. Salama, T. Vos, K.H. Abate, C. Abbafati, M.B. Ahmed, Z. Al-Aly, A. Alkerwi, R. Al-Raddadi, A.T. Amare, A. Amberbir, A.K. Amegah, E. Amini, S.M. Amrock, R.M. Anjana, J. Arnlov, H. Asayesh, A. Banerjee, A. Barac, E. Baye, D.A. Bennett, A.S. Beyene, S. Biadgilign, S. Biryukov, E. Bjertness, D.J. Boneya, I. Campos-Nonato, J.J. Carrero, P. Cecilio, K. Cercy, L.G. Ciobanu, L. Cornaby, S.A. Damtew, L. Dandona, R. Dandona, S.D. Dharmaratne, B.B. Duncan, B. Eshrati, A. Esteghamati, V.L. Feigin, J.C. Fernandes, T. Furst, T.T. Gebrehiwot, A. Gold, P.N. Gona, A. Goto, T.D. Habtewold, K.T. Hadush, N. Hafezi-Nejad, S.I. Hay, M. Horino, F. Islami, R. Kamal, A. Kasaeian, S.V. Katikireddi, A.P. Kengne, C.N. Kesavachandran, Y.S. Khader, Y.H. Khang, J. Khubchandani, D. Kim, Y.J. Kim, Y. Kinfu, S. Kosen, T. Ku, B.K. Defo, G.A. Kumar, H.J. Larson, M. Leinsalu, X. Liang, S.S. Lim, P. Liu, A.D. Lopez, R. Lozano, A. Majeed, R. Malekzadeh, D.C. Malta, M. Mazidi, C. McAlinden, S.T. McGarvey, D.T. Mengistu, G.A. Mensah, G.B.M. Mensink, H.B. Mezgebe, E.M. Mirrakhimov, U.O. Mueller, J.J. Noubiap, C.M. Obermeyer, F.A. Ogbo, M.O. Owolabi, G.C. Patton, F. Pourmalek, M. Qorbani, A. Rafay, R.K. Rai, C.L. Ranabhat, N. Reinig, S. Safiri, J.A. Salomon, J.R. Sanabria, I.S. Santos, B. Sartorius, M. Sawhney, J. Schmidhuber, A.E. Schutte, M.I. Schmidt, S.G. Sepanlou, M. Shamsizadeh, S. Sheikhbahaei, M.J. Shin, R. Shiri, I. Shiue, H.S. Roba, D.A.S. Silva, J.I. Silverberg, J.A. Singh, S. Stranges, S. Swaminathan, R. Tabares-Seisdedos, F. Tadese, B.A. Tedla, B.S. Tegegne, A.S. Terkawi, J.S. Thakur, M. Tonelli, R. Topor-Madry, S. Tyrovolas, K.N. Ukwaja, O.A. Uthman, M. Vaezghasemi, T. Vasankari, V.V. Vlassov, S.E. Vollset, E. Weiderpass, A. Werdecker, J. Wesana, R. Westerman, Y. Yano, N. Yonemoto, G. Yonga, Z. Zaidi, Z.M. Zenebe, B. Zipkin, C.J.L. Murray, Health effects of overweight and obesity in 195 countries over 25 Years. N. Engl. J. Med. 377(1), 13–27 (2017). https://doi.org/10.1056/NEJMoa1614362

    Article  Google Scholar 

  2. B.A. Swinburn, V.I. Kraak, S. Allender, V.J. Atkins, P.I. Baker, J.R. Bogard, H. Brinsden, A. Calvillo, O. De Schutter, R. Devarajan, M. Ezzati, S. Friel, S. Goenka, R.A. Hammond, G. Hastings, C. Hawkes, M. Herrero, P.S. Hovmand, M. Howden, L.M. Jaacks, A.B. Kapetanaki, M. Kasman, H.V. Kuhnlein, S.K. Kumanyika, B. Larijani, T. Lobstein, M.W. Long, V.K.R. Matsudo, S.D.H. Mills, G. Morgan, A. Morshed, P.M. Nece, A. Pan, D.W. Patterson, G. Sacks, M. Shekar, G.L. Simmons, W. Smit, A. Tootee, S. Vandevijvere, W.E. Waterlander, L. Wolfenden, W.H. Dietz, The global syndemic of obesity, undernutrition, and climate change: The Lancet Commission report. Lancet 393(10173), 791–846 (2019). https://doi.org/10.1016/s0140-6736(18)32822-8

    Article  PubMed  Google Scholar 

  3. B. Motamed, A. Eftekharzadeh, F. Hosseinpanah, M. Tohidi, M. Hasheminia, F. Azizi, The relation between changes in thyroid function and anthropometric indices during long-term follow-up of euthyroid subjects: the Tehran Thyroid Study (TTS). Eur. J. Endocrinol. 175(4), 247–253 (2016). https://doi.org/10.1530/EJE-16-0414

    Article  CAS  PubMed  Google Scholar 

  4. J.M. Kim, B.H. Kim, H. Lee, E.H. Kim, M. Kim, J.H. Kim, Y.K. Jeon, S.S. Kim, I.J. Kim, Y.K. Kim, The relationship between thyroid function and different obesity phenotypes in korean euthyroid adults. Diabetes Metab. J. (2019). https://doi.org/10.4093/dmj.2018.0130

  5. M.R. Licenziati, G. Valerio, I. Vetrani, G. De Maria, F. Liotta, G. Radetti, Altered thyroid function and structure in children and adolescents who are overweight and obese: reversal after weight loss. J. Clin. Endocrinol. Metab. 104(7), 2757–2765 (2019). https://doi.org/10.1210/jc.2018-02399

    Article  PubMed  Google Scholar 

  6. F. Santini, P. Marzullo, M. Rotondi, G. Ceccarini, L. Pagano, S. Ippolito, L. Chiovato, B. Biondi, Mechanisms in endocrinology: the crosstalk between thyroid gland and adipose tissue: signal integration in health and disease. Eur. J. Endocrinol. 171(4), R137–R152 (2014). https://doi.org/10.1530/EJE-14-0067

    Article  CAS  PubMed  Google Scholar 

  7. F.M. Collares, T.I.M. Korevaar, A. Hofman, E.A.P. Steegers, R.P. Peeters, V.W.V. Jaddoe, R. Gaillard, Maternal thyroid function, prepregnancy obesity and gestational weight gain—The Generation R Study: a prospective cohort study. Clin. Endocrinol. 87(6), 799–806 (2017). https://doi.org/10.1111/cen.13412

    Article  Google Scholar 

  8. H.M. Al-Musa, Impact of obesity on serum levels of thyroid hormones among euthyroid Saudi Adults. J. Thyroid Res. 2017, 1–5 (2017). https://doi.org/10.1155/2017/5739806

    Article  CAS  Google Scholar 

  9. V. Lundback, K. Ekbom, E. Hagman, I. Dahlman, C. Marcus, Thyroid-stimulating hormone, degree of obesity, and metabolic risk markers in a cohort of swedish children with obesity. Horm. Res. Paediatr. 88(2), 140–146 (2017). https://doi.org/10.1159/000475993

    Article  CAS  PubMed  Google Scholar 

  10. W.K. Cho, H.K. Nam, J.H. Kim, Y.J. Rhie, S. Chung, K.H. Lee, B.K. Suh, Thyroid function in Korean adolescents with obesity: results from the Korea National Health and Nutrition Examination Survey VI (2013–2015). Int J. Endocrinol. 2018, 1–7 (2018). https://doi.org/10.1155/2018/6874395

    Article  CAS  Google Scholar 

  11. A. Sami, M.F. Iftekhar, M.A. Rauf, A. Sher, Subclinical hypothyroidism among local adult obese population. Pak. J. Med. Sci. 34(4), 980–983 (2018). https://doi.org/10.12669/pjms.344.14127

    Article  PubMed  PubMed Central  Google Scholar 

  12. I.M. Bensenor, A.C. Goulart, C. Molina Mdel, E.J. de Miranda, I.S. Santos, P.A. Lotufo, Thyrotropin levels, insulin resistance, and metabolic syndrome: a cross-sectional analysis in the Brazilian Longitudinal Study of Adult Health (ELSA-Brasil). Metab. Syndr. Relat. Disord. 13(8), 362–369 (2015). https://doi.org/10.1089/met.2015.0045

    Article  CAS  PubMed  Google Scholar 

  13. J. Zhang, R. Jiang, L. Li, P. Li, X. Li, Z. Wang, L. Li, W. Teng, Serum thyrotropin is positively correlated with the metabolic syndrome components of obesity and dyslipidemia in chinese adolescents. Int J. Endocrinol. 2014, 289503 (2014). https://doi.org/10.1155/2014/289503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. J.H. Gomez-Zamudio, V. Mendoza-Zubieta, A. Ferreira-Hermosillo, M.A. Molina-Ayala, A. Valladares-Salgado, F. Suarez-Sanchez, J. de Jesus Peralta-Romero, M. Cruz, High thyroid-stimulating hormone levels increase proinflammatory and cardiovascular markers in patients with extreme obesity. Arch. Med. Res. 47(6), 476–482 (2016). https://doi.org/10.1016/j.arcmed.2016.10.007

    Article  CAS  PubMed  Google Scholar 

  15. S. Valdes, C. Maldonado-Araque, A. Lago-Sampedro, J.A. Lillo-Munoz, E. Garcia-Fuentes, V. Perez-Valero, C. Gutierrez-Repiso, E. Garcia-Escobar, A. Goday, I. Urrutia, L. Pelaez, A. Calle-Pascual, E. Bordiu, L. Castano, C. Castell, E. Delgado, E. Menendez, J. Franch-Nadal, S. Gaztambide, J. Girbes, E. Ortega, J. Vendrell, M.R. Chacon, F. Javier Chaves, F. Soriguer, G. Rojo-Martinez, Reference values for TSH may be inadequate to define hypothyroidism in persons with morbid obesity: Di@bet.es study. Obesity 25(4), 788–793 (2017). https://doi.org/10.1002/oby.21796

    Article  CAS  PubMed  Google Scholar 

  16. C. Betry, M.A. Challan-Belval, A. Bernard, A. Charrie, J. Drai, M. Laville, C. Thivolet, E. Disse, Increased TSH in obesity: evidence for a BMI-independent association with leptin. Diabetes Metab. 41(3), 248–251 (2015). https://doi.org/10.1016/j.diabet.2014.11.009

    Article  CAS  PubMed  Google Scholar 

  17. P. Marzullo, A. Minocci, M.A. Tagliaferri, G. Guzzaloni, A. Di Blasio, C. De Medici, G. Aimaretti, A. Liuzzi, Investigations of thyroid hormones and antibodies in obesity: leptin levels are associated with thyroid autoimmunity independent of bioanthropometric, hormonal, and weight-related determinants. J. Clin. Endocrinol. Metab. 95(8), 3965–3972 (2010). https://doi.org/10.1210/jc.2009-2798

    Article  CAS  PubMed  Google Scholar 

  18. J. Rijks, B. Penders, E. Dorenbos, S. Straetemans, W.J. Gerver, A. Vreugdenhil, Pituitary response to thyrotropin releasing hormone in children with overweight and obesity. Sci. Rep. 6, 31032 (2016). https://doi.org/10.1038/srep31032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. M.J. Ford, E.H. Cameron, W.A. Ratcliffe, D.B. Horn, A.D. Toft, J.F. Munro, TSH response to TRH in substantial obesity. Int J. Obes. 4(2), 121–125 (1980)

    CAS  PubMed  Google Scholar 

  20. K. Agbaht, Y. Mercan, S. Kutlu, M.F. Alpdemir, T. Sezgin, Obesity with and without metabolic syndrome: do vitamin D and thyroid autoimmunity have a role? Diabetes Res Clin. Pract. 106(1), 27–34 (2014). https://doi.org/10.1016/j.diabres.2014.08.001

    Article  CAS  PubMed  Google Scholar 

  21. B. Wang, R. Song, W. He, Q. Yao, Q. Li, X. Jia, J.A. Zhang,, Sex differences in the associations of obesity with hypothyroidism and thyroid autoimmunity among chinese adults. Front. Physiol. 9, 1397 (2018). https://doi.org/10.3389/fphys.2018.01397

    Article  PubMed  PubMed Central  Google Scholar 

  22. R. Ghergherehchi, N. Hazhir, Thyroid hormonal status among children with obesity. Therapeutic Adv. Endocrinol. Metab. 6(2), 51–55 (2015). https://doi.org/10.1177/2042018815571892

    Article  CAS  Google Scholar 

  23. M. Rotondi, P. Leporati, A. La Manna, B. Pirali, T. Mondello, R. Fonte, F. Magri, L. Chiovato, Raised serum TSH levels in patients with morbid obesity: is it enough to diagnose subclinical hypothyroidism? Eur. J. Endocrinol. 160(3), 403–408 (2009). https://doi.org/10.1530/EJE-08-0734

    Article  CAS  PubMed  Google Scholar 

  24. W.E. Consultation, Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 363(9403), 157–163 (2004). https://doi.org/10.1016/s0140-6736(03)15268-3

    Article  Google Scholar 

  25. B.F. Zhou, Predictive values of body mass index and waist circumference for risk factors of certain related diseases in Chinese adults—study on optimal cut-off points of body mass index and waist circumference in Chinese adults. Biomed. Environ. Sci. 15, 83–96 (2002)

    PubMed  Google Scholar 

  26. M.K. Kahr, K.M. Antony, M. DelBeccaro, M. Hu, K.M. Aagaard, M.A. Suter, Increasing maternal obesity is associated with alterations in both maternal and neonatal thyroid hormone levels. Clin. Endocrinol. 84(4), 551–557 (2016). https://doi.org/10.1111/cen.12974

    Article  CAS  Google Scholar 

  27. G. Radetti, W. Kleon, F. Buzi, C. Crivellaro, L. Pappalardo, N. di Iorgi, M. Maghnie, Thyroid function and structure are affected in childhood obesity. J. Clin. Endocrinol. Metab. 93(12), 4749–4754 (2008). https://doi.org/10.1210/jc.2008-0823

    Article  CAS  PubMed  Google Scholar 

  28. M. Rotondi, P. Leporati, M.I. Rizza, A. Clerici, G. Groppelli, C. Pallavicini, A. La Manna, R. Fonte, F. Magri, B. Biondi, L. Chiovato, Raised serum TSH in morbid-obese and non-obese patients: effect on the circulating lipid profile. Endocrine 45(1), 92–97 (2014). https://doi.org/10.1007/s12020-013-9928-8

    Article  CAS  PubMed  Google Scholar 

  29. F. Liu, J. Di, H. Yu, J. Han, Y. Bao, W. Jia, Effect of Roux-en-Y gastric bypass on thyroid function in euthyroid patients with obesity and type 2 diabetes. Surg. Obes. Relat. Dis. 13(10), 1701–1707 (2017). https://doi.org/10.1016/j.soard.2017.06.001

    Article  PubMed  Google Scholar 

  30. J.S. Neves, S. Castro Oliveira, P. Souteiro, J. Pedro, D. Magalhaes, V. Guerreiro, R. Bettencourt-Silva, M.M. Costa, A. Cristina Santos, J. Queiros, A. Varela, P. Freitas, D. Carvalho, A. Group, Effect of weight loss after bariatric surgery on thyroid-stimulating hormone levels in patients with morbid obesity and normal thyroid function. Obes. Surg. 28(1), 97–103 (2018). https://doi.org/10.1007/s11695-017-2792-5

    Article  PubMed  Google Scholar 

  31. B. Wolters, N. Lass, T. Reinehr, TSH and free triiodothyronine concentrations are associated with weight loss in a lifestyle intervention and weight regain afterwards in obese children. Eur. J. Endocrinol. 168(3), 323–329 (2013)

    Article  CAS  Google Scholar 

  32. I.M. Janssen, J. Homan, W. Schijns, B. Betzel, E.O. Aarts, F.J. Berends, H. de Boer, Subclinical hypothyroidism and its relation to obesity in patients before and after Roux-en-Y gastric bypass. Surg. Obes. Relat. Dis. 11(6), 1257–1263 (2015). https://doi.org/10.1016/j.soard.2015.02.021

    Article  PubMed  Google Scholar 

  33. J.J. Diez, P. Iglesias, Relationship between thyrotropin and body mass index in euthyroid subjects. Exp. Clin. Endocrinol. Diabetes 119(3), 144–150 (2011). https://doi.org/10.1055/s-0030-1265133

    Article  CAS  PubMed  Google Scholar 

  34. D.S. Montoya-Morales, A.T.-G.M. de Los, L. Alamilla-Lugo, A. Sosa-Caballero, A. Munoz-Solis, M. Jimenez-Sanchez, Alterations of the thyroid function in patients with morbid obesity. Rev. Med Inst. Mex. Seguro Soc. 53(Suppl 1), S18–S22 (2015)

    PubMed  Google Scholar 

  35. S.H. Donders, G.F. Pieters, J.G. Heevel, H.A. Ross, A.G. Smals, P.W. Kloppenborg, Disparity of thyrotropin (TSH) and prolactin responses to TSH-releasing hormone in obesity. J. Clin. Endocrinol. Metab. 61(1), 56–59 (1985). https://doi.org/10.1210/jcem-61-1-56

    Article  CAS  PubMed  Google Scholar 

  36. I. Kyrou, O. Adesanya, N. Hedley, S. Wayte, D. Grammatopoulos, C.L. Thomas, A. Weedall, S. Sivaraman, L. Pelluri, T.M. Barber, V. Menon, H.S. Randeva, M. Tedla, M.O. Weickert, Improved thyroid hypoechogenicity following bariatric-induced weight loss in euthyroid adults with severe obesity-a pilot study. Front Endocrinol. 9, 488 (2018). https://doi.org/10.3389/fendo.2018.00488

    Article  Google Scholar 

  37. L.H. Duntas, B. Biondi, The interconnections between obesity, thyroid function, and autoimmunity: the multifold role of leptin. Thyroid 23(6), 646–653 (2013). https://doi.org/10.1089/thy.2011.0499

    Article  CAS  PubMed  Google Scholar 

  38. M. Zhao, X. Tang, T. Yang, B. Zhang, Q. Guan, S. Shao, F. Xue, X. Zhang, Z. Liu, Z. Yuan, Y. Song, H. Zhang, L. Fang, C. Yu, Q. Li, X. Zhang, L. Gao, C. Xu, J. Zhao, Lipotoxicity, a potential risk factor for the increasing prevalence of subclinical hypothyroidism? J. Clin. Endocrinol. Metab. 100(5), 1887–1894 (2015). https://doi.org/10.1210/jc.2014-3987

    Article  CAS  PubMed  Google Scholar 

  39. M. Sakurai, K. Nakamura, K. Miura, K. Yoshita, T. Takamura, S.Y. Nagasawa, Y. Morikawa, M. Ishizaki, T. Kido, Y. Naruse, M. Nakashima, K. Nogawa, Y. Suwazono, H. Nakagawa, Association between a serum thyroid-stimulating hormone concentration within the normal range and indices of obesity in Japanese men and women. Intern Med. 53(7), 669–674 (2014). https://doi.org/10.2169/internalmedicine.53.1387

    Article  PubMed  Google Scholar 

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Acknowledgements

This research was supported by grant from the National Natural Science Foundation of China (81430020). We appreciate the help and support of all the participants involved in the study.

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The authors’ responsibilities were as follows: L.G. and J.Z. designed research; X.G., Z.H., Y.F., L.L., and D.Z. conducted research; L.Y.G., S.S., and M.Z. provided essential reagents and materials; X.G. and Y.F. analyzed data; X.G. and M.Z. wrote paper; J.Z. and L.G. had primary responsibility for final content. All authors read and approved the final manuscript.

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Correspondence to Liying Guan, Meng Zhao or Jiajun Zhao.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the ethics committee of Shandong Provincial Hospital affiliated to Shandong University (reference number was LCYJ: NO. 2019-002) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Written informed consents were obtained from each subject of epidemiological survey in Ningyang County before entering the survey. Data of health examination population were approved by the ethics committee of Shandong Provincial Hospital affiliated to Shandong University.

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Guo, X., He, Z., Shao, S. et al. Interaction effect of obesity and thyroid autoimmunity on the prevalence of hyperthyrotropinaemia. Endocrine 68, 573–583 (2020). https://doi.org/10.1007/s12020-020-02236-1

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