{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:51:17Z","timestamp":1787028677131,"version":"build-2736575974"},"reference-count":57,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2020,7,3]],"date-time":"2020-07-03T00:00:00Z","timestamp":1593734400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100014269","name":"Uniwersytet Medyczny w Bia\u0142ymstoku","doi-asserted-by":"publisher","award":["SUB\/1\/DN\/20\/002\/1209"],"award-info":[{"award-number":["SUB\/1\/DN\/20\/002\/1209"]}],"id":[{"id":"10.13039\/501100014269","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Hashimoto\u2019s thyroiditis (HT) is one of the most common autoimmune diseases. Although HT is inextricably linked to oxidative stress, there have been no studies assessing salivary redox homeostasis or salivary gland function in patients with HT. This study is the first to compare antioxidant defense and oxidative stress biomarkers in non-stimulated (NWS) and stimulated (SWS) whole saliva and plasma\/erythrocytes of HT patients compared to controls. The study included 45 women with HT in the euthyreosis period as well as an age- and gender-matched control group. We showed that NWS secretion was significantly lower in HT patients compared to healthy controls, similar to salivary amylase activity in NWS and SWS. Catalase and peroxidase activities were considerably higher in NWS and SWS of HT patients, while the concentrations of reduced glutathione and uric acid were significantly lower in comparison with healthy subjects. Total antioxidant potential was significantly lower, while total oxidant status and the level of oxidation products of proteins (advanced glycation end products, advanced oxidation protein products) and lipids (malondialdehyde, lipid hydroperoxides) were significantly higher in NWS, SWS and plasma of HT patients. In conclusion, in both salivary glands of women with HT in euthyreosis, the ability to maintain redox homeostasis was hindered. In HT patients we observed oxidative damage to salivary proteins and lipids; thus, some biomarkers of oxidative stress may present a potential diagnostic value.<\/jats:p>","DOI":"10.3390\/jcm9072102","type":"journal-article","created":{"date-parts":[[2020,7,6]],"date-time":"2020-07-06T09:49:11Z","timestamp":1594028951000},"page":"2102","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":28,"title":["Enhanced Salivary and General Oxidative Stress in Hashimoto\u2019s Thyroiditis Women in Euthyreosis"],"prefix":"10.3390","volume":"9","author":[{"given":"Katarzyna","family":"Morawska","sequence":"first","affiliation":[{"name":"Department of Restorative Dentistry, Medical University of Bialystok, 24A M. Sklodowskiej-Curie Street, 15-276 Bialystok, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5609-3187","authenticated-orcid":false,"given":"Mateusz","family":"Maciejczyk","sequence":"additional","affiliation":[{"name":"Department of Hygiene, Epidemiology and Ergonomics, Medical University of Bialystok, 2c Mickiewicza Street, 15-022 Bialystok, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"\u0141ukasz","family":"Pop\u0142awski","sequence":"additional","affiliation":[{"name":"Department of Radiology, Medical University of Bialystok, 24A M. Sklodowskiej-Curie Street, 15-276 Bialystok, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Pop\u0142awska-Kita","sequence":"additional","affiliation":[{"name":"Department of Endocrinology, Diabetology and Internal Medicine, Medical University of Bialystok, 24A M. Sklodowskiej-Curie Street, 15-276 Bialystok, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4522-4978","authenticated-orcid":false,"given":"Adam","family":"Kr\u0119towski","sequence":"additional","affiliation":[{"name":"Department of Endocrinology, Diabetology and Internal Medicine, Medical University of Bialystok, 24A M. Sklodowskiej-Curie Street, 15-276 Bialystok, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4562-0951","authenticated-orcid":false,"given":"Anna","family":"Zalewska","sequence":"additional","affiliation":[{"name":"Laboratory of Experimental Dentistry, Medical University of Bialystok, 24A M. Sklodowskiej-Curie Street, 15-276 Bialystok, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,7,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/S1568-9972(01)00016-7","article-title":"Iodine: An environmental trigger of thyroiditis","volume":"1","author":"Rose","year":"2002","journal-title":"Autoimmun Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1016\/j.clinbiochem.2012.11.021","article-title":"Enhanced oxidative stress in Hashimoto\u2019s thyroiditis: Inter-relationships to biomarkers of thyroid function","volume":"46","author":"Rostami","year":"2013","journal-title":"Clin. Biochem."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1530\/EJE-15-0617","article-title":"The relationship between oxidative stress and autoimmunity in Hashimoto\u2019s thyroiditis","volume":"173","author":"Ates","year":"2015","journal-title":"Eur. J. Endocrinol"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1080\/13813455.2017.1408660","article-title":"The effect of oxidative stress on the progression of Hashimoto\u2019s thyroiditis","volume":"124","author":"Ates","year":"2018","journal-title":"Arch. Physiol. Biochem."},{"key":"ref_5","first-page":"461","article-title":"Oxidative stress and salivary antioxidants","volume":"50","author":"Maciejczyk","year":"2013","journal-title":"Dent. Med. Probl."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1007\/s12011-010-8625-1","article-title":"A comparative study of the oxidative profile in Graves\u2019 disease, Hashimoto\u2019s thyroiditis, and papillary thyroid cancer","volume":"138","author":"Lassoued","year":"2010","journal-title":"Biol. Trace Elem. Res."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"54","DOI":"10.3923\/ajb.2012.54.58","article-title":"Oxidative stress in anti thyroperoxidase antibody positive hypothyroid patients","volume":"7","author":"Nanda","year":"2012","journal-title":"Asian J. Biochem."},{"key":"ref_8","first-page":"e1","article-title":"Evaluation of Xerostomia and salivary flow rate in Hashimoto\u2019s Thyroiditis","volume":"21","author":"Shirzad","year":"2016","journal-title":"Med. Oral Patol. Oral Cir. Bucal"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Toczewska, J., Konopka, T., Zalewska, A., and Maciejczyk, M. (2020). Nitrosative stress biomarkers in the non-stimulated and stimulated saliva, as well as gingival crevicular fluid of patients with periodontitis: Review and clinical study. Antioxidants, 9.","DOI":"10.3390\/antiox9030259"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"419","DOI":"10.17219\/dmp\/112151","article-title":"Activity of enzymatic antioxidants in periodontitis: A systematic overview of the literature","volume":"56","author":"Toczewska","year":"2019","journal-title":"Dent. Med. Probl."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"5801570","DOI":"10.1155\/2019\/5801570","article-title":"The relationship between the concentration of salivary tyrosine and antioxidants in patients with oral lichen planus","volume":"2019","author":"Darczuk","year":"2019","journal-title":"Oxid. Med. Cell Longev."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1080\/00016357.2019.1578409","article-title":"Evaluation of enzymatic and non-enzymatic antioxidant status and biomarkers of oxidative stress in saliva of patients with oral squamous cell carcinoma and oral leukoplakia: A pilot study","volume":"77","author":"Babiuch","year":"2019","journal-title":"Acta Odont. Scand."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Skutnik-Radziszewska, A., Maciejczyk, M., Flisiak, I., Kolodziej, J.K.U., Kotowska-Rodziewicz, A., Klimiuk, A., and Zalewska, A. (2020). Enhanced inflammation and nitrosative stress in the saliva and plasma of patients with plaque psoriasis. J. Clin. Med., 9.","DOI":"10.3390\/jcm9030745"},{"key":"ref_14","first-page":"9086024","article-title":"Salivary antioxidants and oxidative stress in psoriatic patients: Can salivary total oxidant status and oxidative stress index be a plaque psoriasis biomarker?","volume":"2020","author":"Maciejczyk","year":"2020","journal-title":"Oxid. Med. Cell Longev."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1016\/j.oooo.2012.10.013","article-title":"Rheumatoid arthritis patients with xerostomia have reduced production of key salivary constituents","volume":"115","author":"Zalewska","year":"2013","journal-title":"Oral Surg. Oral Med. Oral Pathol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1111\/jop.12084","article-title":"Salivary antioxidants in patients with systemic sclerosis","volume":"43","author":"Zalewska","year":"2014","journal-title":"J. Oral Pathol. Med."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1493","DOI":"10.3109\/00016357.2013.773071","article-title":"Salivary innate defense system in type 1 diabetes mellitus in children with mixed and permanent dentition","volume":"71","author":"Zalewska","year":"2013","journal-title":"Acta Odont. Scand."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"141","DOI":"10.3109\/10715762.2011.645206","article-title":"Oxidative stress, as measured by protein oxidation, is increased in primary Sj\u00f8gren\u2019s syndrome","volume":"46","author":"Norheim","year":"2012","journal-title":"Free Radic. Res."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.clinbiochem.2014.09.023","article-title":"Markers of oxidative stress in plasma and saliva in patients with multiple sclerosis","volume":"48","author":"Celec","year":"2015","journal-title":"Clin. Biochem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1858","DOI":"10.3899\/jrheum.091451","article-title":"Altered salivary redox homeostasis in patients with systemic sclerosis","volume":"37","author":"Su","year":"2010","journal-title":"J. Rheumatol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1400","DOI":"10.1177\/0961203315593170","article-title":"Alternations of salivary antioxidant enzymes in systemic lupus erythematosus","volume":"24","author":"Zaieni","year":"2015","journal-title":"Lupus"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1016\/S0891-5849(01)00806-1","article-title":"Characterization of the differentiated antioxidant profile of human saliva","volume":"32","author":"Nagler","year":"2002","journal-title":"Free Radic. Biol. Med."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Klimiuk, A., Zalewska, A., Sawicki, R., Knapp, M., and Maciejczyk, M. (2020). Salivary oxidative stress increases with the progression of chronic heart failure. J. Clin. Med., 9.","DOI":"10.3390\/jcm9030769"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1016\/S0076-6879(78)52032-6","article-title":"Microsomal lipid peroxidation","volume":"52","author":"Buege","year":"1978","journal-title":"Methods Enzymol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1136\/ard.61.6.554","article-title":"Classification criteria for Sjogren\u2019s syndrome: A revised version of the European criteria proposed by American-European Consensus Group","volume":"61","author":"Vitali","year":"2002","journal-title":"Ann. Rheum. Dis."},{"key":"ref_26","first-page":"197","article-title":"Studien zur physiologie der tranenabsonderung und tranenabfuhr","volume":"56","author":"Schirmer","year":"1903","journal-title":"Arch. Opthalmol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"3170","DOI":"10.1016\/S0021-9258(19)45228-9","article-title":"The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase","volume":"247","author":"Misra","year":"1972","journal-title":"J. Biol. Chem."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/S0076-6879(84)05016-3","article-title":"Catalase in vitro","volume":"105","author":"Aebi","year":"1984","journal-title":"Methods Enzymol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1016\/0003-9969(86)90095-6","article-title":"Specific assays for peroxidases in human saliva","volume":"31","author":"Baldone","year":"1986","journal-title":"Arch. Oral Biol."},{"key":"ref_30","first-page":"158","article-title":"Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase","volume":"70","author":"Paglia","year":"1967","journal-title":"J. Lab. Clin. Med."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/0003-2697(80)90139-6","article-title":"Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine","volume":"106","author":"Griffith","year":"1980","journal-title":"Anal. Biochem."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/j.clinbiochem.2003.11.015","article-title":"A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation","volume":"37","author":"Erel","year":"2004","journal-title":"Clin. Biochem."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.1016\/j.clinbiochem.2005.08.008","article-title":"A new automated colorimetric method for measuring total oxidant status","volume":"38","author":"Erel","year":"2005","journal-title":"Clin. Biochem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/j.archoralbio.2017.09.006","article-title":"Chronic high-protein diet induces oxidative stress and alters the salivary gland function in rats","volume":"84","author":"Maciejczyk","year":"2017","journal-title":"Arch. Oral Biol."},{"key":"ref_35","first-page":"597","article-title":"Advanced glycation end-products and advanced oxidation protein products in patients with diabetes mellitus","volume":"51","author":"Skrha","year":"2002","journal-title":"Physiol. Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.freeradbiomed.2012.09.038","article-title":"Method for the simultaneous determination of free\/protein malondialdehyde and lipid\/protein hydroperoxides","volume":"59","author":"Grintzalis","year":"2013","journal-title":"Free Radic. Biol. Med."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1042\/bj3600557","article-title":"Hydrogen peroxide-induced production of a 40 kDa immunoreactive thyroglobulin fragment in human thyroid cells: The onset of thyroid autoimmunity?","volume":"360","author":"Duthoit","year":"2001","journal-title":"Biochem. J."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1016\/j.autrev.2008.04.006","article-title":"Autoimmune thyroiditis and ROS","volume":"7","author":"Burek","year":"2008","journal-title":"Autoimmun. Rev."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1016\/j.cbi.2014.10.016","article-title":"Free radicals, reactive oxygen species, oxidative stress and its classification","volume":"224","author":"Lushchak","year":"2014","journal-title":"Chem. Biol. Interact."},{"key":"ref_40","first-page":"922","article-title":"Classification of oxidative stress based on its intensity","volume":"13","author":"Lushchak","year":"2014","journal-title":"Exp. Clin. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1111\/jop.12383","article-title":"Impact of morbid obesity and bariatric surgery on antioxidant\/oxidant balance of the unstimulated and stimulated saliva","volume":"45","author":"Maciejczyk","year":"2016","journal-title":"J. Oral Pathol. Med."},{"key":"ref_42","first-page":"4583742","article-title":"Oxidative damage to the salivary glands of rats with streptozotocin-induced diabetes-temporal study: Oxidative stress and diabetic salivary glands","volume":"2016","author":"Maciejczyk","year":"2016","journal-title":"J. Diabetes Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1016\/j.numecd.2014.01.018","article-title":"Serum uric acid and its relationship with metabolic syndrome and cardiovascular risk profile in patients with hypertension: Insights from the I-DEMAND study","volume":"24","author":"Viazzi","year":"2014","journal-title":"Nutr. Metab. Cardiovasc. Dis."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1021","DOI":"10.17219\/acem\/63030","article-title":"Salivary lipids: A review","volume":"26","author":"Matczuk","year":"2017","journal-title":"Adv. Clin. Exp. Med."},{"key":"ref_45","first-page":"321","article-title":"Salivary gland involvement in rheumatoid arthritis: Salivary peroxidase and the flow rate","volume":"19","author":"Zalewska","year":"2010","journal-title":"Pol. J. Environ. Stud."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/0167-4838(86)90245-1","article-title":"Is thiocyanate peroxidation at equilibrium in vivo?","volume":"870","author":"Pruitt","year":"1986","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/0003-9969(84)90025-6","article-title":"The protective effect of peroxidase and thiocyanate against hydrogen peroxide toxicity assessed by the uptake of [3H]-thymidine by human gingival fibroblasts cultured in vitro","volume":"29","author":"Tenovuo","year":"1984","journal-title":"Arch. Oral Biol."},{"key":"ref_48","first-page":"268","article-title":"Lactoperoxidase and thiocyanate protect cultured mammalian cells against hydrogen peroxide toxicity","volume":"61","author":"Hanstrom","year":"1983","journal-title":"Med. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1024\/0300-9831\/a000008","article-title":"Hypoglycemic and antioxidant effects of honey supplementation in streptozotocin-induced diabetic rats","volume":"80","author":"Erejuwa","year":"2010","journal-title":"Int. J. Vitam. Nutr. Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1517\/17425255.2011.577738","article-title":"Reversible and irreversible protein glutathionylation: Biological and clinical aspects","volume":"7","author":"Cooper","year":"2011","journal-title":"Expert Opin. Drug Metab. Toxicol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"736837","DOI":"10.1155\/2012\/736837","article-title":"Glutathione homeostasis and functions: Potential targets for medical interventions","volume":"2012","author":"Lushchak","year":"2012","journal-title":"J. Amino Acids"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1585","DOI":"10.1002\/art.10315","article-title":"Suppression of tumor necrosis factor alpha-induced matrix metalloproteinase 9 production in human salivary gland acinar cells by cepharanthine occurs via down-regulation of nuclear factor kappaB: A possible therapeutic agent for preventing the destruction of the acinar structure in the salivary glands of Sjogren\u2019s syndrome patients","volume":"46","author":"Azuma","year":"2002","journal-title":"Arthr. Rheum."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1095","DOI":"10.1007\/s00405-008-0598-8","article-title":"Salivary gland biometry in female patients with eating disorders","volume":"265","author":"Bozzato","year":"2008","journal-title":"Eur. Arch. Otorhinolaryngol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1067\/moe.2001.114756","article-title":"Quantitative analysis of normal major salivary glands using computed tomography","volume":"92","author":"Heo","year":"2001","journal-title":"Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1254\/jjp.87.117","article-title":"Lowered susceptibility of muscarinic receptor involved in salivary secretion of streptozotocin-induced diabetic rats","volume":"87","author":"Watanabe","year":"2001","journal-title":"Jpn. J. Pharmacol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1016\/S0945-053X(98)90116-0","article-title":"A novel and simple immunocapture assay for determination of gelatinase-B (MMP-9) activities in biological fluids: Saliva from patients with Sjogren\u2019s syndrome contain increased latent and active gelatinase-B levels","volume":"17","author":"Hanemaaijer","year":"1998","journal-title":"Matrix Biol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1159\/000199729","article-title":"Adrenergic effects on secretion of amylase from the rat salivary glands","volume":"41","author":"Kirkegaard","year":"1988","journal-title":"Digestion"}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/9\/7\/2102\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:47:11Z","timestamp":1760176031000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/9\/7\/2102"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,7,3]]},"references-count":57,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2020,7]]}},"alternative-id":["jcm9072102"],"URL":"https:\/\/doi.org\/10.3390\/jcm9072102","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,7,3]]}}}