Abstract
Objective
Whether breastfeeding influences thyroid function and autoimmunity is not elucidated. We examined the association of history of breastfeeding with thyroid hormones and thyroperoxidase antibody (TPOAb).
Design
Cross-sectional study of data from the 2013–2015 Korea National Health and Nutrition Examination Survey.
Methods
A total of 816 postmenopausal women were stratified into three groups according to the duration of breastfeeding and number of breastfed children. Thyroid hormones levels, TPOAb titers, and the prevalence of hypothyroidism and TPOAb positivity were evaluated in each group.
Results
Subjects with a history of prolonged breastfeeding had lower levels of thyrotropin (TSH) and TPOAb than the others. After adjusting for multiple confounding factors, the estimated means of TSH and TPOAb were associated with cumulative duration of breastfeeding. Duration of breastfeeding per child was associated with TSH levels, and number of breastfed children was associated with TPOAb titers. The odds ratio (OR) of hypothyroidism was significantly lower in group for ≥36 months of cumulative duration of breastfeeding, and the OR of TPOAb positivity was significantly lower in group with ≥3 breastfed children. In addition, duration of breastfeeding and the number of breastfed children were linearly correlated with log TSH and TPOAb each other in the multivariate model.
Conclusions
The present study showed that prolonged breastfeeding was inversely associated with TSH and the prevalence of hypothyroidism. Moreover, TPOAb and the prevalence of TPOAb positivity were inversely associated with number of breastfed children. These results indicate that breastfeeding may exert a protective effect on thyroid function and autoimmunity.
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References
M.P. Vanderpump, W.M. Tunbridge, J.M. French, D. Appleton, D. Bates, F. Clark, J. Grimley Evans, D.M. Hasan, H. Rodgers, F. Tunbridge et al. The incidence of thyroid disorders in the community: a twenty-year follow-up of the Whickham Survey. Clin. Endocrinol. 43(1), 55–68 (1995). https://doi.org/10.1111/j.1365-2265.1995.tb01894.x
J.G. Hollowell, N.W. Staehling, W.D. Flanders, W.H. Hannon, E.W. Gunter, C.A. Spencer, L.E. Braverman, Serum TSH, T(4), and thyroid antibodies in the United States population (1988 to 1994): National Health and Nutrition Examination Survey (NHANES III). J. Clin. Endocrinol. Metab. 87(2), 489–499 (2002). https://doi.org/10.1210/jcem.87.2.8182
K.I. Kennedy, C.M. Visness, Contraceptive efficacy of lactational amenorrhoea. Lancet 339(8787), 227–230 (1992). https://doi.org/10.1016/0140-6736(92)90018-x
D.A. Battin, R.P. Marrs, P.M. Fleiss, D.R. Mishell Jr., Effect of suckling on serum prolactin, luteinizing hormone, follicle-stimulating hormone, and estradiol during prolonged lactation. Obstet. Gynecol. 65(6), 785–788 (1985)
Z. Ben-Rafael, J.F. Struass, 3rd, B. Arendash-Durand, L.J. Mastroianni, G.L. Flickinger, Changes in thyroid function tests and sex hormone binding globulin associated with treatment by gonadotropin. Fertil. Steril. 48(2), 318–320 (1987). https://doi.org/10.1016/s0015-0282(16)59363-7
D. Manole, B. Schildknecht, B. Gosnell, E. Adams, M. Derwahl, Estrogen promotes growth of human thyroid tumor cells by different molecular mechanisms. J. Clin. Endocrinol. Metab. 86(3), 1072–1077 (2001). https://doi.org/10.1210/jcem.86.3.7283
G.G. Chen, A.C. Vlantis, Q. Zeng, C.A. van Hasselt, Regulation of cell growth by estrogen signaling and potential targets in thyroid cancer. Curr. Cancer Drug Targets 8(5), 367–377 (2008). https://doi.org/10.2174/156800908785133150
P.L. Panuganti, S.N. Hinkle, S. Rawal, L.G. Grunnet, Y. Lin, A. Liu, A.C.B. Thuesen, S.H. Ley, S.F. Olesen, C. Zhang, Lactation duration and long-term thyroid function: a study among women with gestational diabetes. Nutrients 10(7), 938 (2018). https://doi.org/10.3390/nu10070938
C.M. Grimaldi, J. Cleary, A.S. Dagtas, D. Moussai, B. Diamond, Estrogen alters thresholds for B cell apoptosis and activation. J. Clin. Invest. 109(12), 1625–1633 (2002). https://doi.org/10.1172/jci14873
K. Lelu, S. Laffont, L. Delpy, P.E. Paulet, T. Perinat, S.A. Tschanz, L. Pelletier, B. Engelhardt, J.C. Guery, Estrogen receptor alpha signaling in T lymphocytes is required for estradiol-mediated inhibition of Th1 and Th17 celldifferentiation and protection against experimental autoimmune encephalomyelitis. J. Immunol. 187(5) 2386–2393 (2011). https://doi.org/10.4049/jimmunol.1101578
N. Talal, Sjogren’s syndrome: historical overview and clinical spectrum of disease. Rheum. Dis. Clin. N. Am. 18(3), 507–515 (1992)
R. Will, L. Edmunds, J. Elswood, A. Calin, Is there sexual inequality in ankylosing spondylitis? A study of 498 women and 1202 men. J. Rheumatol. 17(12), 1649–1652 (1990)
W.J. Fessel, Systemic lupus erythematosus in the community. Incidence, prevalence, outcome, and first symptoms; the high prevalence in black women. Arch. Intern. Med. 134(6), 1027–1035 (1974)
A. Linos, J.W. Worthington, W.M. O’Fallon, L.T. Kurland, The epidemiology of rheumatoid arthritis in Rochester, Minnesota: a study of incidence, prevalence, and mortality. Am. J. Epidemiol. 111(1), 87–98 (1980). https://doi.org/10.1093/oxfordjournals.aje.a112878
C. Confavreux, M. Hutchinson, M.M. Hours, P. Cortinovis-Tourniaire, T. Moreau, Rate of pregnancy-related relapse in multiple sclerosis. Pregnancy in Multiple Sclerosis Group. N. Engl. J. Med. 339(5), 285–291 (1998). https://doi.org/10.1056/nejm199807303390501
J. Li, R.W. McMurray, Effects of estrogen receptor subtype-selective agonists on autoimmune disease in lupus-prone NZB/NZW F1 mouse model. Clin. Immunol. 123(2), 219–226 (2007). https://doi.org/10.1016/j.clim.2007.01.008
D. Alpizar-Rodriguez, N. Pluchino, G. Canny, C. Gabay, A. Finckh, The role of female hormonal factors in the development of rheumatoid arthritis. Rheumatology (Oxford, England) 56(8), 1254–1263 (2017). https://doi.org/10.1093/rheumatology/kew318
M. Pikwer, U. Bergstrom, J.A. Nilsson, L. Jacobsson, G. Berglund, C. Turesson, Breast feeding, but not use of oral contraceptives, is associated with a reduced risk of rheumatoid arthritis. Ann. Rheum. Dis. 68(4), 526–530 (2009). https://doi.org/10.1136/ard.2007.084707
E.W. Karlson, L.A. Mandl, S.E. Hankinson, F. Grodstein, Do breast-feeding and other reproductive factors influence future risk of rheumatoid arthritis? Results from the Nurses’ Health Study. Arthritis Rheum. 50(11), 3458–3467 (2004). https://doi.org/10.1002/art.20621
A. Langer-Gould, J.B. Smith, K. Hellwig, E. Gonzales, S. Haraszti, C. Koebnick, A. Xiang, Breastfeeding, ovulatory years, and risk of multiple sclerosis. Neurology 89(6), 563–569 (2017). https://doi.org/10.1212/wnl.0000000000004207
W.G. Kim, W.B. Kim, G. Woo, H. Kim, Y. Cho, T.Y. Kim, S.W. Kim, M.H. Shin, J.W. Park, H.L. Park, K. Oh, J.H. Chung, Thyroid stimulating hormone reference range and prevalence of thyroid dysfunction in the Korean population: Korea national health and nutrition examination survey 2013 to 2015. Endocrinol. Metab. (Seoul, Korea) 32(1), 106–114 (2017). https://doi.org/10.3803/EnM.2017.32.1.106
M. Kotopouli, T. Stratigou, G. Antonakos, G.S., Christodoulatos, I., Karampela, M. Dalamaga, Early menarche is independently associated with subclinical hypothyroidism: a cross-sectional study. Horm. Mol. Biol. Clin. Investig. 38(1) (2019). https://doi.org/10.1515/hmbci-2018-0079
L.E. Braverman, Iodine and the thyroid: 33 years of study. Thyroid 4(3), 351–356 (1994). https://doi.org/10.1089/thy.1994.4.351
P. Laurberg, K.M. Pedersen, A. Hreidarsson, N. Sigfusson, E. Iversen, P.R. Knudsen, Iodine intake and the pattern of thyroid disorders: a comparative epidemiological study of thyroid abnormalities in the elderly in Iceland and in Jutland, Denmark J. Clin. Endocrinol. Metab. 83(3), 765–769 (1998). https://doi.org/10.1210/jcem.83.3.4624
M.J. Kang, I.T. Hwang, H.R. Chung, Excessive iodine intake and subclinical hypothyroidism in children and adolescents aged 6-19 years: results of the sixth Korean National Health and Nutrition Examination Survey, 2013-2015. Thyroid 28(6), 773–779 (2018). https://doi.org/10.1089/thy.2017.0507
H.I. Kim, H.K. Oh, S.Y. Park, H.W. Jang, M.H. Shin, S.W. Kim, T.H. Kim, J.H. Chung, Urinary iodine concentration and thyroid hormones: Korea National Health and Nutrition Examination Survey 2013-2015. Eur. J. Nutr. 58(1), 233–240 (2019). https://doi.org/10.1007/s00394-017-1587-8
H.R. Chung, C.H. Shin, S.W. Yang, C.W. Choi, B.I. Kim, Subclinical hypothyroidism in Korean preterm infants associated with high levels of iodine in breast milk. The. J. Clin. Endocrinol. Metab. 94(11), 4444–4447 (2009). https://doi.org/10.1210/jc.2009-0632
K.J. Park, L.M. Peterson, Beliefs, practices, and experiences of Korean women in relation to childbirth. Health Care Women Int. 12(2), 261–269 (1991). https://doi.org/10.1080/07399339109515946
J. Choi, H.S. Kim, D.J. Hong, H. Lim, J.H. Kim, Urinary iodine and sodium status of urban Korean subjects: a pilot study. Clin. Biochem. 45(7-8), 596–598 (2012). https://doi.org/10.1016/j.clinbiochem.2012.02.018
S. Hwang, E.Y. Lee, W.K. Lee, D.Y. Shin, E.J. Lee, Correlation between iodine intake and thyroid function in subjects with normal thyroid function. Biol. Trace Elem. Res. 143(3), 1393–1397 (2011). https://doi.org/10.1007/s12011-011-8997-x
S. Kim, Y.S. Kwon, J.Y. Kim, K.H. Hong, Y.K. Park, Association between iodine nutrition status and thyroid disease-related hormone in Korean adults: Korean National Health and Nutrition Examination Survey VI (2013-2015). Nutrients 11(11), 2757 (2019). https://doi.org/10.3390/nu11112757
H. Kim, H.N. Lee, J. Ha, Association high-iodine-containing seaweed soup consumption after birth and subclinical hypothyroidism in Korean women: Korea National Health and Nutrition Examination Survey IV (2013–2015). Int. J. Thyroidol. 12(2), 105–112 (2019)
Acknowledgements
We thank all the participants for enthusiastically participating in this study.
Funding
This study was supported by a grant (no. 2019–374) from the Asan Institute for Life Sciences, Asan Medical Center, Seoul, Korea.
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All procedures involving human participants were performed in accordance with the ethical standards of the institutional and/or national research committee, and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The Institutional Review Board of the Korea Centers for Disease Control and Prevention approved the KNHANES (2013–07CON-03-4C and 2013–12EXP-03-5C).
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Kim, SW., Lee, JH., Shon, HS. et al. Association of breastfeeding with thyroid function and autoimmunity in postmenopausal women. Endocrine 71, 130–138 (2021). https://doi.org/10.1007/s12020-020-02385-3
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DOI: https://doi.org/10.1007/s12020-020-02385-3