Abstract
Hypothyroidism is a common endocrine disorder that influences body weight and several aspects of energy metabolism. Today, herbal medicine is focused on the treatment of diseases, especially endocrine disorders. Artemisia dracunculus (Tarragon) is a member of the Asteraceae (Compositae) family. The aim of the present study was to examine the effects of Artemisia dracunculus aqueous extract on serum thyroid hormones, lipid profile, leptin, adiponectin, and antioxidant factors in adult male rats with propylthiouracil (PTU)-induced hypothyroidism. Forty-eight mature male Albino Wistar rats were housed in standard cages. Hypothyroidism was induced in the rats by the administration of PTU in drinking water to a final concentration of 500 mg/L. This study lasted for 90 days. The animals were divided into six experimental groups (eight rats per each group): (1) normal control; (2) hypothyroid rats + levothyroxine, as positive control (4 μg/100 g/day); (3) hypothyroid rats, as negative control; (4) hypothyroid rats + tarragon aqueous extract (100 mg/kg); (5) hypothyroid rats + tarragon aqueous extract (200 mg/kg); and (6) hypothyroid rats + tarragon aqueous extract (300 mg/kg). Blood samples were obtained using cardiac puncture. In blood samples, thyroid hormones (triiodothyronine (T3), free triiodothyronine (fT3), thyroxine (T4), and free thyroxine (fT4)), thyroid-stimulating hormone (TSH), leptin, adiponectin, antioxidant elements (malondialdehyde (MDA), total antioxidant capacity (TAC), glutathione (GSH)), and lipid profile (triglyceride (TG), cholesterol, high-density lipoprotein (HDL), low-density lipoprotein (LDL)) were measured. The serum level of thyroid hormones (T3, fT3, T4, and fT4) decreased in the negative control group compared to the normal control group, but the tarragon extract improved their levels. The levels of fT3 and fT4 were higher in 300 mg/kg tarragon treatment (P < 0.05). In addition, tarragon extracts decreased the elevated TSH level in the negative control rats. Tarragon extract at dose 100 mg/kg reduced the TSH level considerably (P < 0.05). Leptin level was not influenced in any of the experimental groups while adiponectin serum concentration decreased in the negative control group. Tarragon extract could not increase the adiponectin level in the treatment groups (P > 0.05). The tarragon extract increased the TAC level at dose 200 mg/kg and the GSH level in a dose-dependent manner (P < 0.05). The MDA level decreased in the negative control rats, and high dose of tarragon treatment decreased the MDA level compare to the normal control group. The tarragon extract increased the lipid profile. In conclusion, the tarragon aqueous extract could improve thyroid hormones profile in hypothyroidism. Thus, it could be used as co-treatment for hypothyroidism, but further studies are needed to confirm these data.
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References
Alzerjawi JMAASJS (2013) Effect of propylthiouracil-induced hypothyroidism on reproductive effeciency of adult male rats. Basrah J Vet Res 12(2):113–121
Ashwini S, Bobby Z, Sridhar MG, Cleetus CC (2017) Insulin plant (Costus pictus) extract restores thyroid hormone levels in experimental hypothyroidism. Pharm Res 9(1):51–59. https://doi.org/10.4103/0974-8490.199766
Behbahani BA, Shahidi F, Tabatabaei Yazdi F, Mortazavi SA, Mohebbi M (2017) Antioxidant activity and antimicrobial effect of tarragon (Artemisia dracunculus) extract and chemical composition of its essential oil. J Food Meas Charact 11(2):847–863. https://doi.org/10.1007/s11694-016-9456-3
Bhanja S, Chainy GBN (2010) PTU-induced hypothyroidism modulates antioxidant defence status in the developing cerebellum. Int J Dev Neurosci 28(3):251–262. https://doi.org/10.1016/j.ijdevneu.2010.01.005
Bloomer RJ, Canale RE, Pischel I (2011) Effect of an aqueous Russian tarragon extract on glucose tolerance in response to an oral dextrose load in non-diabetic men. Nutr Diet Suppls 3:43–49
Cano-Europa E, Blas-Valdivia V, Franco-Colin M, Gallardo-Casas CA, Ortiz-Butrón R (2011) Methimazole-induced hypothyroidism causes cellular damage in the spleen, heart, liver, lung and kidney. Acta Histochem 113(1):1–5. https://doi.org/10.1016/j.acthis.2009.07.004
Cefalu WT, Ye J, Zuberi A, Ribnicky DM, Raskin I, Liu Z, Lefevre M (2008) Botanicals and the metabolic syndrome. Am J Clin Nutr 87(2):481S–487S
Chaalal A, Poirier R, Blum D, Gillet B, Le Blanc P, Basquin M, Enderlin V (2014) PTU-induced hypothyroidism in rats leads to several early neuropathological signs of Alzheimer’s disease in the hippocampus and spatial memory impairments. Hippocampus 24(11):1381–1393. https://doi.org/10.1002/hipo.22319
Chaker L, Bianco AC, Jonklaas J, Peeters RP (2017) Hypothyroidism. Lancet 390(10101):1550–1562. https://doi.org/10.1016/S0140-6736(17)30703-1
Chakera AJ, Pearce SHS, Vaidya B (2012) Treatment for primary hypothyroidism: current approaches and future possibilities. Drug Des Dev Ther 6:1–11
Chanchal DK, Gupta A, Suchita W, Bina G (2016) Herbal drugs for thyroid. Int J Pharm Bio Sci 6(1):62–70
Chatzitomaris A, Hoermann R, Midgley JE, Hering S, Urban A, Dietrich B, Dietrich JW (2017) Thyroid allostasis–adaptive responses of thyrotropic feedback control to conditions of strain, stress, and developmental programming. Front Endocrinol 8:163 Chatzitomaris et al., 2017
Chen Y, Wu X, Wu R, Sun X, Yang B, Wang Y, Xu Y (2016) Changes in profile of lipids and adipokines in patients with newly diagnosed hypothyroidism and hyperthyroidism. Sci Rep 6(1):26174. https://doi.org/10.1038/srep26174
Cheserek MJ, Wu GR, Ntazinda A, Shi YH, Shen LY, Le GW (2015) Association between thyroid hormones, lipids and oxidative stress markers in subclinical hypothyroidism. J Med Biochem 34(3):323–331
Deshpande UR, Joseph LJ, Patwardhan UN, Samuel AM (2002) Effect of antioxidants (vitamin C, E and turmeric extract) on methimazole induced hypothyroidism in rats. Indian J Exp Biol 40(6):735–738
Duntas LH (2002) Thyroid disease and lipids. Thyroid 12(4):287–293
Durić K, Kovač-Bešović E, Nikšić H, Sofić E (2013) AntioxidantactivityofwaterextractsandessentialoilofArtemisa Dracunculus L., Asteraceae. Med J Aust 19(2):94–99
Duric K, Kovac-Besovic EE, Niksic H, Muratovic S, Sofic E (2015) Anticoagulant activity of some Artemisia dracunculus leaf extracts. Bosn J Basic Med Sci 15(2):9–14
Escobar-Morreale HF, Botella-Carretero JI, de Escobar GM (2015) Treatment of hypothyroidism with levothyroxine or a combination of levothyroxine plus L-triiodothyronine. Best Pract Res Clin Endocrinol Metab 29(1):57–75
Fernández-Real JM, López-Bermejo A, Casamitjana R, Ricart W (2003) Novel interactions of adiponectin with the endocrine system and inflammatory parameters. J Clin Endocrinol Metab 88(6):2714–2718
Ferreira E, Silva AE, Serakides R, Gomes AES, Cassali GD (2007) Model of induction of thyroid dysfunctions in adult female mice. Arquivo Brasileiro de Medicina Veterinaria e Zootecnia 59(5):1245–1249. https://doi.org/10.1590/S0102-09352007000500022
Goli Movahed GA, Mehraban Sang Atash M (2007) Comparision of antioxidant and anti-radical activities of edible leafy vegetables methanolic extract. J Med Plants 8(1):64–71
Hwang JH, Jung HW, Kang SY, Kang AN, Ma JN, Meng XL, Hwang MS, Park YK (2018) Therapeutic effects of acupuncture with MOK, a polyherbal medicine, on PTU-induced hypothyroidism in rats. Exp Ther Med 16(1):310–320. https://doi.org/10.3892/etm.2018.6190
Joshi B, Singh S, Saini A, Gupta S, Vanishree BJ (2018) A study of lipid peroxidation and total antioxidant capacity in hyperthyroid and hypothyroid female subjects. Galore Int J Health Sci Res 3(4):1–8
Kim KJ, Kim BY, Mok JO, Kim CH, Kang SK, Jung CH (2015) Serum concentrations of ghrelin and leptin according to thyroid hormone condition, and their correlations with insulin resistance. Endocrinol Metab 30(3):318–325. https://doi.org/10.3803/EnM.2015.30.3.318
Kirk-Ballard H, Wang ZQ, Acharya P, Zhang XH, Yu Y, Kilroy G, Floyd ZE (2013) An extract of Artemisia dracunculus L.inhibits ubiquitin-proteasome activity and preserves skeletal muscle mass in a murine model of diabetes. PLoS One 8(2):e57112. https://doi.org/10.1371/journal.pone.0057112
Kokkinos A, Mourouzis I, Kyriaki D, Pantos C, Katsilambros N, Cokkinos DV (2007) Possible implications of leptin, adiponectin and ghrelin in the regulation of energy homeostasis by thyroid hormone. Endocrine 32(1):30–32. https://doi.org/10.1007/s12020-007-9002-5
Kostoglou-Athanassiou I, Ntalles K (2010) Hypothyroidism - new aspects of an old disease. Hippokratia 14:82–87
Lima Gonçalves CF, de Souza dos Santos MC, Ginabreda MG, Soares Fortunato R, Pires de Carvalho D, Freitas Ferreira AC (2013) Flavonoid routin increases thyroid iodide uptake in rats. PLoS One 8(9):e73908. https://doi.org/10.1371/journal.pone.0073908
Liu YY, Schultz JJ, Brent GA (2003) A thyroid hormone receptor $α$ gene mutation (P398H) is associated with visceral adiposity and impaired catecholamine-stimulated lipolysis in mice. J Biol Chem 278(40):38913–38920
Mahmoodi M, Koohpeyma F, Saki F, Maleksabet A (2019) The protective effect of Zataria multiflora Boiss. hydroalcoholic extract on TNF-α production, oxidative stress, and insulin level in streptozotocin-induced diabetic rats. Avicenna J Phytomed 9(1):72
McAninch EA, Bianco AC (2016) The history and future of treatment of hypothyroidism. Ann Intern Med 164(1):50–56. https://doi.org/10.7326/M15-1799
Méndez-del Villar M, Puebla-Pérez AM, Sánchez-Peña MJ, González-Ortiz LJ, Martínez-Abundis E, González-Ortiz M (2016) Effect of Artemisia dracunculusadministration on glycemic control, insulin sensitivity, and insulin secretion in patients with impaired glucose tolerance. J Med Food 19(5):481–485. https://doi.org/10.1089/jmf.2016.0005
Mirazi N, Abdolmaleki N, Mahmoodi M (2013) Study of Salvia Officinalishydroethanolic extract on serum thyroid hormone levels in hypothyroid male rat. Sci J Hamadan Univ Med Sci 19(4):27–35
Mohiuddin D, Ganai BA, Chishti MZ, Ahmad F, Dar JS (2014) Phytochemical studies on the extract and essential oils of Artemisia dracunculus L.(Tarragon). African J Plant Sci 8(1):72–75
Nazeri S, Rostamian M, Hedayati M (2014) Impact of thyroid dysfunction on antioxidant capacity, super oxide dismutase and catalase activity. Zahedan J Res Med Sci 16(1):51–54
Nazifi S, Saeb M, Sepehrimanesh M, Poorgonabadi S (2012) The effects of wild pistachio oil on serum leptin, thyroid hormones, and lipid profile in female rats with experimental hypothyroidism. Comp Clin Pathol 21(5):851–857. https://doi.org/10.1007/s00580-011-1188-5
Obolskiy D, Pischel I, Feistel B, Glotov N, Heinrich M (2011) Artemisia dracunculus L. (tarragon): a critical review of its traditional use, chemical composition, pharmacology, and safety. J Agric Food Chem 59(21):11367–11384. https://doi.org/10.1021/jf202277w
Pantos C, Malliopoulou V, Mourouzis I, Sfakianoudis K, Tzeis S, Doumba P (2003) Propylthiouracil-induced hypothyroidism is associated with increased tolerance of the isolated rat heart to ischaemia-reperfusion. J Endocrinol 178(3):427–436
Parmar HS, Kar A (2009) Protective role of Mangifera indica, Cucumis melo and Citrullus vulgaris peel extracts in chemically induced hypothyroidism. Chem Biol Interact 177(3):254–258. https://doi.org/10.1016/j.cbi.2008.11.006
Petrulea MS, Duncea I, Hazi G, Dragotoiu G, Decea N, Mure\csan A (2010) Oxidative stress in experimental hypothyroidism: effect of vitamin E supplementation. Clujul Med 83(2): 245–249
Rajabian A, Hassanzadeh Khayyat M, Emami SA, Tayarani-Najaran Z, Rahimzadeh Oskooie R, Asili J (2016) Phytochemical evaluation and antioxidant activity of essential oil, and aqueous and organic extracts of Artemisia dracunculus. Jundishapur J Nat Pharm Prod 12(1):e32325. https://doi.org/10.5812/jjnpp.32325
Ribnicky DM, Poulev A, Watford M, Cefalu WT, Raskin I (2006) Antihyperglycemic activity of Tarralin™, an ethanolic extract of Artemisia dracunculus L. Phytomedicine 13(8):550–557. https://doi.org/10.1016/j.phymed.2005.09.007
Rizzo LFL, Mana DL, Serra HA (2017) Drug-induced hypothyroidism. Medicina (Buenos Aires) 77(5):394–404. https://doi.org/10.1016/S0362-5486(76)80011-8
Santi A, Baldissareli J, Murussi C, Dias G, de Menezes C, Zanini D, Loro V (2014) Effects of quercetin on oxidative stress biomarkers in methimazole – induced hypothyroid rats. Exp Clin Endocrinol Diabetes 122(09):533–539. https://doi.org/10.1055/s-0034-1376968
Saxena V, Dharamveer GR, Saraf SA (2012) Ficus carica leaf extract in regulation of thyroidism using ELISA technique. Asian J Pharm Clin Res 5(2):44–48
Schlenker EH (2012) Effects of hypothyroidism on the respiratory system and control of breathing: human studies and animal models. Respir Physiol Neurobiol 181(2):123–131. https://doi.org/10.1016/j.resp.2012.02.007
Seifi S, Tabandeh MR, Nazifi S, Saeb M, Shirian S, Sarkoohi P (2012) Regulation of adiponectin gene expression in adipose tissue by thyroid hormones. J Physiol Biochem 68(2):193–203. https://doi.org/10.1007/s13105-011-0131-1
Sesmilo G, Casamitjana R, Halperin I, Gomis R, Vilardell E (1998) Role of thyroid hormones on serum leptin levels. Eur J Endocrinol 139(4):428–430
Shahraki MR, Mirshekari H, Samadi Z (2015) The nociceptive and anti-inflammatory effects of Artemisia dracunculus L. aqueous extract on fructose fed male rats. Evid Based Complement Alternat Med 2015:1–5. https://doi.org/10.1155/2015/895417
Shahriyary L, Yazdanparast R (2007) Inhibition of blood platelet adhesion, aggregation and secretion by Artemisia dracunculus leaves extracts. J Ethnopharmacol 114(2):194–198. https://doi.org/10.1016/j.jep.2007.07.029
Sharafati Chaleshtori R, Rokni N, Razavilar V, Rafieian Kopaei M (2013) The evaluation of the antibacterial and antioxidant activity of tarragon (Artemisia dracunculus L.) essential oil and its chemical composition. Jundishapur J Microbiol 6(9):e7877. https://doi.org/10.5812/jjm.7877
Shokri Z, Khoshbin M, Koohpayeh A, Abbasi N, Bahmani F, Rafieian-Kopaei M, Beyranvand F (2018) Thyroid diseases: pathophysiology and new hopes in treatment with medicinal plants and natural antioxidants. Int J Green Pharm 12(03):S476
Sourour DA (2014) Curcumin induces apoptosis in thyroid cells in rats: possible role of caspase 3. IJAR 2(1):790–801
Tabassum W, Kullu AR, Sinha MP (2013) Effects of leaf extracts of Moringa oleifera on regulation of hypothyroidism and lipid profile. Bioscan 8(2):665–669
Teixeira B, Marques A, Ramos C, Neng NR, Nogueira JMF, Saraiva JA, Nunes ML (2013) Chemical composition and antibacterial and antioxidant properties of commercial essential oils. Ind Crop Prod 43:587–595. https://doi.org/10.1016/j.indcrop.2012.07.069
Tuncel M (2017) Thyroid stimulating hormone receptor. Mol Imaging Radionuclide Ther 26(Suppl 1):87–91
Valcavi R, Zini M, Peino R, Casanueva FF, Dieguez C (1997) Influence of thyroid status on serum immunoreactive leptin levels. J Clin Endocrinol Metab 82(5):1632–1634
Wanjari P, Jayadeepa RM (2012) A novel in-silico drug designing approach for identification of natural compounds for treatment of hypothyroid. Int Proc Chem Biol Environ Eng 31:12–16
Weinoehrl S, Feistel B, Pischel I, Kopp B, Butterweck V (2012) Comparative evaluation of two different Artemisia dracunculus L. cultivars for blood sugar lowering effects in rats. Phytother Res 26(4):625–629
Yu H, Yang Y, Zhang M, Lu H, Zhang J, Wang H, Cianflone K (2006) Thyroid status influence on adiponectin, acylation stimulating protein (ASP) and complement C3 in hyperthyroid and hypothyroid subjects. Nutr Metab 3(1):13. https://doi.org/10.1186/1743-7075-3-13
Zhang H, Dong Y, Su Q (2016) Perinatal hypothyroidism modulates antioxidant defence status in the developing rat liver and heart. Can J Physiol Pharmacol 95(2):185–189
Acknowledgments
The authors would like to thank the Research Council of Shiraz University and School of Veterinary Medicine, Shiraz University, for their financial and technical support of this study.
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This study was funded by Shiraz University (grant number: 71-GR-VT-5).
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The trial was approved by the members of the state commission on animal ethics, Shiraz University, Shiraz, Iran (IACUC no: 4687/63). Additionally, the advice of European Council Directive (86/609/EC) of November 24, 1986, concerning the protection of animals, were fully considered for trial procedures.
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Mohammadi, M.M., Saeb, M. & Nazifi, S. Experimental hypothyroidism in adult male rats: the effects of Artemisia dracunculus aqueous extract on serum thyroid hormones, lipid profile, leptin, adiponectin, and antioxidant factors. Comp Clin Pathol 29, 485–494 (2020). https://doi.org/10.1007/s00580-019-03080-0
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DOI: https://doi.org/10.1007/s00580-019-03080-0