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Impaired Endothelium-Dependent Vasodilatation in Subclinical Hypothyroidism: Beneficial Effect of Levothyroxine Therapy
Abstract
Subclinical hypothyroidism (sHT) is associated with enhanced cardiovascular risk. To test the hypothesis that patients with sHT are characterized by endothelial dysfunction and impaired nitric oxide (NO) availability, in 14 patients [serum cholesterol, 218 +/- 41 mg/dl (5.6 +/- 0.9 mM)] and 28 euthyroid subjects, subdivided into groups A and B [serum cholesterol, 170 +/- 19 mg/dl (4.4 +/- 0.5 mM) and 217 +/- 21 mg/dl (5.6 +/- 0.5 mM), respectively], we studied the forearm blood flow (strain-gauge plethysmography) response to intrabrachial acetylcholine, an endothelium-dependent vasodilator, at baseline and during infusion of N(G)-monomethyl-L-arginine (L-NMMA), a NO synthase inhibitor. Response to sodium nitroprusside and minimal forearm vascular resistances were also evaluated. In sHT patients, vasodilation to acetylcholine was reduced, compared with group B (+358 +/- 29% vs. +503 +/- 19%, P = 0.0003) and group A (663 +/- 65%, P = 0.02 vs. group B and P = 0.0002 vs. sHT). L-NMMA blunted the vasodilation to acetylcholine in groups A and B (49.1 +/- 6.3% and 42.7 +/- 5.5% maximal forearm blood flow reduction, respectively, P < 0.0001 vs. acetylcholine), whereas it was ineffective in sHT patients (12.8 +/- 2.5%). Response to sodium nitroprusside and minimal vascular resistances were similar. In sHT (n = 9) patients, 6 months of euthyroidism by levothyroxine replacement increased acetylcholine-vasodilation and restored L-NMMA inhibition. Patients with sHT are characterized by endothelial dysfunction resulting from a reduction in NO availability, an alteration partially independent of dyslipidemia and reversed by levothyroxine supplementation.
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“Both hyperlipidemia and thyroid antibodies are thought to reduce expression of endothelial nitric oxide synthase, thereby impairing vasodilation (15).”
From Thyroid Hormones and Cardiovascular Function and Diseases (2018) · cites this paper as [15]
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“(5) It was also revealed that endothelial dysfunction in subclinical hypothyroidism could be partially reversed by levothyroxine supplementation.(5) However, even though systemic vascular resistance is increased, blood pressure may remain nearly stable in subclinical hypothyroidism because of diminished cardiac output.”
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“In humans, the vasodilating effect of acetylcholine was significantly reduced in subclinical hypothyroidism, compared with healthy subjects, and 6 months of euthyroidism by levothyroxine replacement increased acetylcholine-vasodilation and restored NG-monomethyl-l-arginine (a competitive, inactive analogue of l-argini…”
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Güngör, Â., Palabıyık, Ş. S., Bayraktutan, Z., Dursun, H., Gökkaya, N., Bilen, A., & Bilen, H. (2016) · Endocrine Research · doi:10.3109/07435800.2015.1135443 · Cited by 13
“In addition, it has been proven that levothyroxine treatment has an inhibitor effect on atherosclerosis and endothelial dysfunction existing in these patients (1,6).”
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Ma, X., Wang, F., Zhen, X., Zhao, L., Li, F., Dong, Z., Chen, W., & Zhou, X. (2020) · International Journal of Endocrinology · doi:10.1155/2020/3161730 · Cited by 13
Abdominal Obesity Is Characterized by Higher Pulse Pressure: Possible Role of Free Triiodothyronine
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“endothelial dysfunction may be more prevalent in hypothyroid patients [26, 27], and increased diastolic blood pressure and higher arterial stiffening are present in subclinical hypothyroid patients [28].”
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“In hyperthyroidism, these compounds affect the cardiac output 50 to 300% higher than that of normal healthy persons, while hypothyroidism shows opposite cardiovascular effects, and cardiac output may fall by 30 to 50% [55].”
BackgroundReview of Postoperative Care for Heart Transplant Recipients
Hwang, N. C., & Sivathasan, C. (2022) · Journal of Cardiothoracic and Vascular Anesthesia · doi:10.1053/j.jvca.2022.09.083 · Cited by 13
Neonatal hypothyroidism does not increase Sertoli cell proliferation in iNOS−/− mice
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The effect of overt and subclinical hypothyroidism on the development of non-dipper blood pressure.
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Subclinical hypothyroidism ups the risk of vascular complications in type 2 diabetes
Mohamed, G. A., & Elsayed, A. M. (2017) · Alexandria Journal of Medicine · doi:10.1016/j.ajme.2016.10.003 · Cited by 10
“Also, thyroid hormone deficiency can also damage vascular function directly.(25,26) Furthermore, several researchers have stated that SCH impairs the relaxation of vascular smooth muscle cells, thereby inducing increased arterial stiffness and systemic vascular resistance(25), as well as changes in endothelial functio…”
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“Patients with subclinical hypothyroidism have decreased NO bioavailability and endothelial dysfunction, and endothelial function was normalized by treatment with thyroid hormone [250].”
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BackgroundSubclinical Hypothyroidism – What is Responsible for its Association with Cardiovascular Disease?
Sorisky, A. (2016) · touchREVIEWS in Endocrinology · doi:10.17925/ee.2016.12.02.96 · Cited by 10
“Elevations in interleukin (IL)-6 and C-reactive protein (CRP) have been detected in SH patients.(6,7) Metabolic effects include higher levels of free fatty acids (FFA), which can also lead to inflammatory cellular actions.”
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“Interestingly, increased TSH levels have been found to associate with endothelial dysfunction and to decrease nitric oxide (NO) availability in the endothelium [9].”
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Heim, M., Nixon, I. J., Emmerson, E., & Callanan, A. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.997288 · Cited by 12
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“The second and more accepted mechanism is the chronic stimulation of the immune system by Hashimoto thyroiditis, the persistence of only elevated ESR and thyroid Abs after achieving euthyroidism proves a role for Hashimoto thyroiditis in the residual endothelial dysfunction.(64) 2.”
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Dardano, A., Caraccio, N., & Monzani, F. (2006) · Thyroid · doi:10.1089/thy.2006.16.200 · Cited by 9
“We had previously demonstrated a reversible alteration of endothelium dependent vasodilatation and reduced nitric oxide availability in SH patients (6).”
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Changes in cerebral blood flow velocity in patients with hypothyroidism
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Hypothyroidism and Heart Failure: Epidemiology, Pathogenetic Mechanisms & Therapeutic Rationale
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“But many other atherosclerotic modifiable risk factors like high concentrations of cholesterol; accelerated atherosclerosis, coronary artery disease and impaired endothelial derived relaxation factor (nitric oxide) are also affected [25,26].”
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Ipadeola, A., Nkwocha, G., & Adeleye, J. O. (2013) · Indian Journal of Endocrinology and Metabolism · doi:10.4103/2230-8210.119562 · Cited by 9
“Many previous studies have also documented similar resolution of symptoms with treatment, corroborating the fi nding that replacement of thyroxine restores the impairment of endothelium-derived vasodilation from diminished nitric oxide.[5-7] It is recommended that all patients with overt hypothyroidism and subclinical…”
Das, G. C., Taylor, P. N., Abusahmin, H., Ali, A., Tennant, B. P., Geen, J., & Okosieme, O. E. (2018) · Annals of Clinical Biochemistry International Journal of Laboratory Medicine · doi:10.1177/0004563218797979 · Cited by 9
“the euthyroid range can contribute to increase in systemic vascular resistance and arterial stiffness needs to be confirmed by experimental studies but such trends have been already noted in patients with SCH.(10,30) Thyroid function has a substantial impact on glucose and lipid metabolism and has been linked to compo…”
Ippolito, S., Ippolito, R., Peirce, C., Esposito, R., Arpaia, D., Santoro, C., Pontieri, G., Cocozza, S., Galderisi, M., & Biondi, B. (2016) · Thyroid · doi:10.1089/thy.2016.0082 · Cited by 8
“Thyroid hormone deficiency reduces NO availability and increases system vascular resistance and arterial stiffness, thereby resulting in endothelial dysfunction (6–8).”
Hypothyroïdie fruste et qualité de vie chez des femmes hypercholestérolémiques de plus de 50 ans
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“L’HTF a également été associée à une augmentation de l’épaisseur intima-média carotide et à des anomalies de la vasomotricité réversibles avec le traitement thyroxinique [24,25].”
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Hypothyroidism and Metabolic Syndrome
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Pearce, S. H. S., Vaisman, M., & Wémeau, J.-L. (2012) · European Thyroid Journal · doi:10.1159/000335964 · Cited by 7
Thyrotropin Levels and Risk of Fatal Coronary Heart Disease
Björn, O., Bjøro, T., Ivar, T., Nilsen, L., Gunnell, D., & VATTEN, L. J. (2017) · Cited by 7
Subclinical Hypothyroidism and the Heart: The Beat Goes On
Danzi, S. E., & Klein, I. L. (2012) · Thyroid · doi:10.1089/thy.2012.2203.ed · Cited by 7
“Taddei and colleagues (10) showed that impaired endothelial dependent vasodilatation in subclinical hypothyroidism responded to thyroid hormone treatment through alterations in a nitric oxide–mediated pathway.”
Evsen, A., & Oylumlu, M. (2024) · Acta cardiologica. Supplementum · doi:10.1080/00015385.2024.2375486 · Cited by 6
Aydın, A., Vural, P., Oruç, Ç. U., Doğru‐Abbasoğlu, S., Özderya, A., Karadağ, B., & Uysal, M. (2014) · International Immunopharmacology · doi:10.1016/j.intimp.2014.04.023 · Cited by 6
Regulators of thymic stromal lymphopoietin production by human adipocytes
Ma, L., Zhen, J., & Sorisky, A. (2020) · Cytokine · doi:10.1016/j.cyto.2020.155284 · Cited by 6
Mohn, A., Michele, S. D., Faricelli, R., Martinotti, S., & Chiarelli, F. (2005) · European Journal of Endocrinology · doi:10.1530/eje.1.02008 · Cited by 6
“Furthermore, thyroxine replacement therapy started early in patients with subclinical hypothyroidism reduces the risk of hyperlipidemia and atherosclerotic heart disease ( 2 ).”
BackgroundKłubo-Gwieździńska, J., Bernet, V. J., & Wartofsky, L. (2013) · Humana Press eBooks · doi:10.1007/978-1-62703-314-5_6 · Cited by 6
Nath, M., Gupta, B., Rai, M., & Singh, S. K. (2017) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2017.07.028 · Cited by 6
Wang, Z., Ding, J., Chen, J., Ding, Y., Ji, X., & Meng, R. (2020) · International Journal of Neuroscience · doi:10.1080/00207454.2020.1782901 · Cited by 6
Subclinical hypothyroidism is associated with albuminuria in Japanese nondiabetic subjects
Toda, A., Hara, S., Tsuji, H., & Arase, Y. (2020) · Endocrine · doi:10.1007/s12020-020-02220-9 · Cited by 6
Thyroid Hormones (T3 and T4) and Their Effects on the Cardiovascular System
Gelen, V., Şengül, E., & Kükürt, A. (2023) · IntechOpen eBooks · doi:10.5772/intechopen.109623 · Cited by 5
Skin microvascular reactivity in patients with hypothyroidism
Mihor, A., Gergar, M., Gaberšček, S., & Lenasi, H. (2016) · Clinical Hemorheology and Microcirculation · doi:10.3233/ch-162062 · Cited by 5
Awari, D. W., Dhanasekaran, M., Mudrakola, H. V., Morales, D. J. V., Weingarten, T. N., & Šprung, J. (2021) · Journal of Cardiothoracic and Vascular Anesthesia · doi:10.1053/j.jvca.2021.02.025 · Cited by 5
Elevated serum thyrotropin levels and endothelial dysfunction in a prospective hemodialysis cohort
You, A. S., Budoff, M. J., Zeb, I., Ahmadi, N., Novoa, A., Flores, F. R., Hamal, S. A., Kinninger, A., Dailing, C., Nakata, T., et al. (2021) · Hemodialysis International · doi:10.1111/hdi.12964 · Cited by 6
“, levothyroxine) over a 3–6 month period reverses endothelial dysfunction in patients with subclinical hypothyroidism.(38,42) To date, a growing body of evidence suggests that alterations in thyroid markers are associated with worse endothelial function in advanced CKD and ESRD patients.”
Background2023 Korean Thyroid Association Management Guidelines for Patients with Subclinical Hypothyroidism
Chung, H. K., Ku, E. J., Yoo, W. S., Kang, Y. E., Kim, K. J., Kim, B. H., Kim, T. Y., Park, Y. J., Ahn, C. H., Yoon, J. H., et al. (2023) · International Journal of Thyroidology · doi:10.11106/ijt.2023.16.1.32 · Cited by 6
Gluvic, Z. M., Sudar-Milovanovic, E. M., Samardzic, V. S., Obradovic, M. M., Jevremović, D., Radenković, S., & Isenović, E. R. (2019) · Medical Hypotheses · doi:10.1016/j.mehy.2019.109299 · Cited by 6
Hipotiroidismo subclínico: Actualización
Sáez, J. G., Martínez, F. C., Fernández, P. G., & Despaigne, D. N. (2005) · Revista cubana de endocrinología · Cited by 5
Valverde, L., & Virla, E. G. (2007) · Americanae (AECID Library) · Cited by 5
Aspects of Treatment of Subclinical Hypothyroidism
Lazarus, J. H. (2007) · Thyroid · doi:10.1089/thy.2006.0286 · Cited by 5
Thyroid function in pediatric patients with juvenile idiopathic arthritis
Valenzise, M., D’Amico, F., Tripodi, E., Zirilli, G., Alibrandi, A., Gallizzi, R., Sutera, D., Cafarella, G., Lugarà, C., & Wasniewska, M. G. (2023) · Endocrine · doi:10.1007/s12020-023-03600-7 · Cited by 4
Abasilim, C., Persky, V., Sargis, R. M., Argos, M., Daviglus, M. L., Freels, S. A., Cai, J., Tsintsifas, K., Isasi, C. R., Peters, B. A., et al. (2024) · Journal of the Endocrine Society · doi:10.1210/jendso/bvae088 · Cited by 4
“Thyroid dysfunction observed in hypothyroidism impacts BP regulation through decreased production of nitric oxide and endothelial dysfunction and impaired relaxation of vascular smooth muscle (77).”
BackgroundÜnsal, İ. Ö., Topaloğlu, O., Çakır, E., Bozkurt, N. Ç., Karbek, B., Güngüneş, A., Arslan, M. S., Tutal, E., Uçan, B., Demirci, T., et al. (2014) · Journal of Medical Disorders · doi:10.7243/2053-3659-2-1 · Cited by 4
“Hypothyroidism is accompanied by endothelial dysfunction and impaired nitric oxide production, which are also encountered in the early stage of atherosclerosis [41-44].”
BackgroundCardiovascular Risk and Mild Thyroid Hormone Deficiency: Are there some Differences in the Elderly?
Pasqualetti, G. (2014) · Journal of Hematology & Thromboembolic Diseases · doi:10.4172/2329-8790.1000e116 · Cited by 3
“In this setting, conflicting data are still existing on the association between sHT and CHD: some studies reporting increased risk [4,11-12], some decreased [13] and some the lack of any association [14-21].”
BackgroundOutcomes of Cardiac Resynchronization Therapy in Patients with Hypothyroidism and Heart Failure
Yang, M., Li, X., Morris, J. C., Liang, J., Deshmukh, A. J., Hodge, D. O., Li, Y., & Cha, Y. (2020) · BMC Cardiovascular Disorders · doi:10.1186/s12872-020-01693-w · Cited by 4
“Numerous studies have reported improvement in vascular and cardiac function and arterial stiffness in patients with SH [26, 27].”
BackgroundBraiteh, N., Senyondo, G. D., Rahman, M. F., Chaudhry, R., & Kashou, H. E. (2021) · American Journal of Case Reports · doi:10.12659/ajcr.929573 · Cited by 4
“Vascular resistance is increased due to lack of T4 effect on initiating the release of endothelial-derived relaxing factor [4].”
BackgroundThyroid Abnormalities in Heart Failure
Danzi, S. E., & Klein, I. L. (2022) · Cardiology Clinics · doi:10.1016/j.ccl.2021.12.002 · Cited by 4
Hirata, A. H. D. L., Rocha, L. A. D. J., da Silva, V. A., de Almeida, R. J., Bacigalupo, L. D. S., Varela, P., Martins, L. D. O., Pesquero, J. B., Dellê, H., & Camacho, C. P. (2020) · Scientific Reports · doi:10.1038/s41598-020-63040-5 · Cited by 4
Cardiogenic Shock in Hypothyroidism
Ashwath, M. L., Kang, G. S., Cunningham, M., & Adler, D. S. (2006) · Southern Medical Journal · doi:10.1097/01.smj.0000215857.47925.fc · Cited by 4
“The mechanism of action is felt to be direct vascular smooth muscle relaxation along with an increase in endothelial cell production of nitric oxide.(3,4) Although reported, overt heart failure is uncommon in hypothyroidism despite slowed diastolic relaxation and increased vascular resistance, probably due to lowered…”
Background
Metadata
- Authors
- Taddei, S., Caraccio, N., Virdis, A., Dardano, A., Versari, D., Ghiadoni, L., Salvetti, A., Ferrannini, E., & Monzani, F.
- Affiliations
- University of Pisa (IT)
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2003-08-01
- Volume
- 88
- Issue
- 8
- Pages
- 3731-3737
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2060930755
- Cited by
- 431
- References
- 43
- Citations by year
- 2026: 8 · 2025: 6 · 2024: 14 · 2023: 15 · 2022: 24 · 2021: 14 · 2020: 27 · 2019: 19 · 2018: 19 · 2017: 12 · 2016: 24 · 2015: 17 · 2014: 34 · 2013: 26 · 2012: 26
- FWCI
- 9.77
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Disorders and Treatments
- Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Health and Disease Prevention
- Keywords
- subclinical hypothyroidism, endothelial dysfunction, endothelium-dependent vasodilation, nitric oxide bioavailability, levothyroxine, acetylcholine, L-NMMA, forearm blood flow, dyslipidemia, cardiovascular risk, sodium nitroprusside
- MeSH terms
- Acetylcholine, Adult, Endothelium, Vascular, Enzyme Inhibitors, Female, Humans, Hypothyroidism, Iodide Peroxidase, Lipids, Lipoproteins, LDL, Male, Nitric Oxide, Nitroprusside, Regional Blood Flow, Thyroglobulin, Thyroid Hormones, Thyroiditis, Autoimmune, Thyroxine, Vascular Resistance, Vasodilation, Vasodilator Agents, Nitric Oxide Synthase, omega-N-Methylarginine, Nitric Oxide Donors, Nitric Oxide Synthase Type III
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