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Journal of Clinical Endocrinology & Metabolism , doi:10.1210/jc.2006-1552
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The Journal of Clinical Endocrinology & Metabolism Vol. 92, No. 1 250-254
Copyright © 2007 by The Endocrine Society

Acute Effects of Triiodothyronine on Endothelial Function in Human Subjects

Raffaele Napoli, Vincenzo Guardasole, Valentina Angelini, Emanuela Zarra, Daniela Terracciano, Carolina D’Anna, Margherita Matarazzo, Ugo Oliviero, Vincenzo Macchia and Luigi Saccà

Departments of Internal Medicine and Cardiovascular Sciences (R.N., V.G., V.A., E.Z., C.D., M.M., U.O., L.S.) and Clinical Pathology (D.T., V.M.), University Federico II, 80131 Naples, Italy

Address all correspondence and requests for reprints to: Dr. R. Napoli, Department of Internal Medicine, Via Pansini, 80131 Napoli, Italy. E-mail: napoli{at}unina.it.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Context: Thyroid hormone regulates several cardiovascular functions, and low T3 levels are frequently associated with cardiovascular diseases. Whether T3 exerts any acute and direct effect on endothelial function in humans is unknown.

Objective: Our objective was to clarify whether acute changes in serum T3 concentration affect endothelial function.

Design, Setting, and Subjects: Ten healthy subjects (age, 24 ± 1 yr) participated in a double-blind, placebo-controlled trial at a university hospital.

Interventions: T3 (or placebo) was infused for 7 h into the brachial artery to raise local T3 to levels observed in moderate hyperthyroidism. Vascular reactivity was tested by intraarterial infusion of vasoactive agents.

Main Outcome Measures: We assessed changes in forearm blood flow (FBF) measured by plethysmography.

Results: FBF response to the endothelium-dependent vasodilator acetylcholine was enhanced by T3 (P = 0.002 for the interaction between T3 and acetylcholine). The slopes of the dose-response curves were 0.41 ± 0.06 and 0.23 ± 0.04 ml/dl·min/µg in the T3 and placebo study, respectively (P = 0.03). T3 infusion had no effect on the FBF response to sodium nitroprusside. T3 potentiated the vasoconstrictor response to norepinephrine (P = 0.006 for the interaction). Also, the slopes of the dose-response curves were affected by T3 (1.95 ± 0.77 and 3.83 ± 0.35 ml/dl·min/mg in the placebo and T3 study, respectively; P < 0.05). The increase in basal FBF induced by T3 was inhibited by NG-monomethyl-L-arginine.

Conclusions: T3 exerts direct and acute effects on the resistance vessels by enhancing endothelial function and norepinephrine-induced vasoconstriction. The data may help clarify the vascular impact of the low T3 syndrome and point to potential therapeutic strategies.


   Introduction
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 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
THE CARDIOVASCULAR SYSTEM is a specific target of thyroid hormone (TH), and when TH secretion is chronically altered, this is accompanied by profound changes in cardiovascular hemodynamics (1, 2). In particular, hyperthyroidism induces a high-output state, with a marked fall in systemic vascular resistance (SVR), whereas hypothyroidism causes opposite changes. More recent studies demonstrate that vascular reactivity is exaggerated in patients with hyperthyroidism because of enhanced sensitivity of the endothelial component (3). Conversely, impaired endothelial function is associated with hypothyroidism, even if the disease is present only at a subclinical level (4, 5, 6). Overall, the data available support a physiological role for TH in the long-term control of endothelial function and vascular homeostasis.

A low-T3 syndrome may occur in acute diseases and is characterized by depressed cardiac function and elevated SVR (7, 8, 9, 10, 11). It was hypothesized that acute correction of the low T3 levels might be beneficial to the cardiovascular hemodynamics (12, 13, 14, 15, 16, 17, 18). However, the precise link between T3 and the altered hemodynamics remains elusive because the effects of acute elevations in serum T3 concentration on human vascular physiology have never been explored in depth. In particular, there is no information as to whether acute changes in circulating T3 are able to exert any effect on endothelial function and the vascular sensitivity to vasoactive agents. The present study was thus designed to address this specific question.


   Subjects and Methods
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 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

The study was performed on 10 healthy volunteers, recruited from the medical population of the medical school (six male, four female, 23.9 ± 0.6 yr of age; body mass index, 23.6 ± 1.6 kg/m2; arterial blood pressure, 119 ± 6/74 ± 5 mm Hg). Informed consent was obtained from all subjects, and the study protocol was approved by the Ethics Committee of the Federico II University School of Medicine.

Experimental procedures

The study design was double blinded and placebo controlled, with each subject serving as his/her own control. The test (T3) and control study were performed in random order and separated by a 3- to 4-wk interval. In the test study, T3 was infused into the brachial artery and forearm hemodynamics were monitored for 240 min. Then the responses of forearm blood flow (FBF) to vasoactive test substances were measured while keeping the infusion of T3 going. In the control study, the protocol was the same except that placebo was infused instead of T3. The dose of T3 was 40 ng/min. This dose was chosen in pilot experiments as the one able to raise free T3 (fT3) concentration in the forearm circulation to moderate hyperthyroidism values. T3 vials for human use (Thyrotardin) were provided by Henning GMBH, Sanofi-Synthelabo, Berlin, Germany.

All the experiments were performed in the morning in a quiet room kept at 22–24 C. A plastic cannula (20 gauge) was inserted into the brachial artery of the nondominant arm under local anesthesia and used for the infusion of the test substances and the monitoring of arterial blood pressure. Systolic and diastolic blood pressure and heart rate were recorded by a transducer connected to the arterial cannula. FBF was measured by a strain-gauge plethysmograph (Hokanson 045 EC4; PMS Instruments, Maidenhead, UK). The data were monitored continuously with McLab software. Additional details of the procedure have been previously published (3, 19). Each subject underwent the following stepwise infusions into the brachial artery in this order: 1) acetylcholine (Ach) infused at a rate of 15, 30, and 45 µg per liter of forearm per min (µg/liter·min) to assess endothelium-mediated vasodilation; 2) sodium nitroprusside (NP), a direct nitric oxide donor, infused at the rate of 1, 3, and 9 µg/liter·min to assess non-endothelium-mediated vasodilation; 3) norepinephrine infused at a rate of 140, 280, and 560 µg/liter·min to assess the vascular sensitivity to sympathetic stimulation; and 4) NG-monomethyl-L-arginine (L-NMMA), a competitive inactive analog of L-arginine, infused at the rate of 1 mg/liter·min to assess the role of endothelial NO release in the maintenance of the basal vascular tone. Test substances were infused in the same order in all the subjects and the infusion of each substance started only when the effect on FBF of the previous infusion was dissolved and baseline FBF restored. Each dose of the test substances was infused for 5.5 min, and FBF was measured during the last 1.5 min of infusion. At least 30 min of washout time was allowed between each substance. The infusion rates were adjusted according to the forearm volume of each subject, measured by water displacement. FBF was measured simultaneously in both arms to ensure that no systemic effects occurred during the experiment. Each FBF value represents the mean of six consecutive measurements performed at 10-sec intervals.

Assays and calculations

T3 plasma level was measured by RIA. Forearm vascular resistance (FVR) was measured as the ratio of mean arterial blood pressure to FBF. Comparison between placebo and T3 was performed by a two-way ANOVA for repeated measures (version 12.0; SPSS Inc., Chicago, IL). Comparison between the slopes of the dose-response curves was performed by paired t test. Results are expressed as the mean ± SEM.


   Results
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 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
The study was well tolerated by all subjects without any systemic reaction. In particular, arterial systolic and diastolic blood pressure and heart rate did not change from their basal values (Table 1Go).


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  		TABLE 1. Effects of intrabrachial T3 infusion on FBF, mean blood pressure, heart rate, and vascular resistance

 
Local, intrabrachial T3 infusion raised the plasma venous concentration of fT3 in the ipsilateral forearm from 3.23 ± 0.19 to 10.42 ± 0.88 pg/ml. The systemic fT3 concentration, as measured in the control arm, was not affected by local T3 infusion (3.24 ± 0.2 and 3.92 ± 0.23 pg/ml at baseline and at the end of the infusion period, respectively). In the placebo study, the fT3 concentration in the venous plasma of the infused forearm was 3.24 ± 0.2 pg/ml basally and remained unchanged throughout the study. Similarly, TSH plasma levels remained unchanged during T3 infusion (1.17 ± 0.12 and 1.41 ± 0.22 µU/ml, at 240 min in controls and during T3 infusion, respectively, P value was nonsignificant).

FBF was very similar in the T3 and placebo studies in the basal state (Table 1Go). During intraarterial T3 infusion, FBF increased progressively and reached values that were significantly higher than those in the placebo study at 120 min and thereafter. This was due to a significant fall in SVR, because arterial blood pressure remained totally unchanged.

Figure 1Go depicts the dose-response curve to the endothelium-dependent vasodilator Ach. The increment of FBF observed in the T3 study was much more pronounced as compared with placebo (P = 0.014 for the treatment effect by ANOVA for repeated measures). The values reached at the highest Ach level were 17.5 ± 2.7 and 10.2 ± 1.7 ml/100 m·min in the test and placebo study, respectively (P = 0.04). The dynamics of the response was also profoundly affected by T3, as evidenced by the significant interaction between T3 and Ach (P = 0.002) and the markedly steeper slope of the T3 dose response compared with that in the placebo study (0.41 ± 0.06 and 0.23 ± 0.04 ml/dl·min/µg, respectively, P = 0.03).


Figure 1
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  		FIG. 1. FBF response to infusion of Ach into brachial artery in placebo- and T3-treated subjects (n = 10). T3 or placebo was infused for 4 h, and then vascular reactivity was tested while keeping the infusion going. Data (mean ± SE) were analyzed by ANOVA for repeated measures. P = 0.014 for the effect of T3, and P = 0.002 for the interaction between T3 and Ach. Comparison between slopes was performed by the paired t test. The units of the slopes are ml/dl·min/µg.

 
Figure 2Go depicts the response of FBF to NP, an endothelium-independent vasodilator. The dose-response curves were virtually identical in the T3 and placebo studies (P value nonsignificant for both the treatment effect and the interaction). Consistently, the calculated slopes of the two curves were almost identical (1.59 ± 0.19 and 1.66 ± 0.15 ml/dl·min/µg in the placebo and T3 study, respectively).


Figure 2
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  		FIG. 2. Response of FBF to infusion of NP in placebo- and T3-treated subjects (n = 10). The response to NP was assessed 30 min after the end of the Ach test. Data (mean ± SE) were analyzed by ANOVA for repeated measures. P = 0.21 for the effect of T3, and P = 0.81 for the interaction between T3 and NP. Comparison between slopes was performed by the paired t test. The units of the slopes are ml/dl·min/µg.

 
As shown in Fig. 3Go, T3 also affected the response of FBF to norepinephrine. In the control study, norepinephrine induced a progressive but moderate decrease in FBF. In contrast, the fall in FBF was 2-fold greater in the subjects receiving T3 than in the placebo study (P = 0.019 for the treatment effect, and P = 0.006 for the interaction). Accordingly, the slopes of the dose-response curves were 1.95 ± 0.77 and 3.83 ± 0.35 ml/dl·min/mg in the placebo and T3 groups, respectively (P < 0.05).


Figure 3
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  		FIG. 3. Response of FBF to infusion of norepinephrine in placebo- and T3-treated subjects (n = 10). The response to norepinephrine was assessed 30 min after the end of the NP test. Data were analyzed by ANOVA for repeated measures. P = 0.019 for the effect of norepinephrine, and P = 0.006 for the interaction between norepinephrine and T3. Comparison between slopes was performed by the paired t test. The units of the slopes are ml/dl·min/mg.

 
Inhibition of basal NO bioavailability by intraarterial administration of L-NMMA caused FBF to rapidly fall. However, the decrease of FBF was more marked during T3 infusion than in the placebo study (–1.47 ± 0.2 and –2.43 ± 0.5 ml/dl·min in the placebo and T3 study, respectively; P < 0.05).

The intrabrachial T3 infusion did not affect systemic hemodynamics, as demonstrated by the unchanged heart rate and arterial blood pressure. In addition, FBF and FVR in the contralateral arm did not change from their basal values throughout the study period.


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Current knowledge about the cardiovascular actions of T3 is mainly deduced from studies of disease states of altered TH secretion or from animal models of chronic TH excess or deficiency. No attempt was made before the present study to explore the impact on vascular physiology of an acute elevation of T3 concentration in human subjects. We tried to answer the question by using the forearm perfusion technique. T3 concentration was acutely raised to levels comparable to those seen in patients with hyperthyroidism of intermediate severity. In addition, T3 concentration was raised only locally, in the forearm circulation, and this allows assessment of the direct effect of T3 on vascular function, without the intervention of systemic factors, either chemical or hemodynamic in nature, potentially able to affect vascular reactivity. The main findings of our study are 1) T3 increments to hyperthyroid values cause a significant fall in FVR by an endothelium-dependent mechanism; 2) T3 markedly potentiates Ach-induced vasodilation but is without effect on the vasodilatory response to NP, which indicates that T3 effects are entirely mediated by the endothelium and do not involve the vascular smooth muscle cell (VSMC) component; and 3) the sensitivity of the resistance vessels to the vasoconstrictory effect of norepinephrine is enhanced by T3.

Previous experiments using mesenteric resistance vessels showed that the vasorelaxing effect of TH was impaired by pretreatment with an arginine analog that prevented endothelial nitric oxide production (20). Similarly, in another study on renal artery rings, endothelium-dependent relaxation to Ach was enhanced 36 h after T3 treatment (21). The present data are consistent with those in vitro observations regarding the role played by the endothelium in mediating the vascular effects of TH. At variance with these data, other studies have supported a role for VSMCs in mediating the vasodilating effect of T3. For instance, the vasorelaxing effect of T3 in isolated resistance vessels was attenuated but not abolished by endothelial denudation of the arteries (22), suggesting activation by T3 of both the endothelial and the nonendothelial component of vasodilation. In another study performed in isolated VSMCs, it was reported that TH was able to cause vasorelaxation (23). The reasons for the difference between our findings and some of the previous studies indicating also a role of VSMC is not clearly apparent and may entail differences among species and in vitro vs. in vivo data. However, taking the data altogether, one thing that emerges clearly is that whenever the vascular effects of TH were tested in human models (normal subjects, hyperthyroidism, overt hypothyroidism, or subclinical hypothyroidism), the changes in vascular reactivity always involved exclusively the endothelial component (3, 4, 6, 24). The current study documents the ability of acute T3 increments to enhance the activity of endothelial NO synthase, as evidenced by the attenuation of FBF after exposure to the arginine antagonistic agent L-NMMA. This finding is consistent with previous studies in chronically hyperthyroid patients as well as experimental studies in various animal models (3, 25).

T3 mainly acts by binding to specific nuclear receptors, so regulating transcription of target genes. In addition, T3 may also activate extranuclear, nongenomic mechanisms, by which it regulates the activity of plasma membrane ion channels. Examples are provided by the well-known T3 effects to enhance myocardial contractility, to regulate the contractile state of VSMCs, and to stimulate glucose uptake (26, 27, 28). The current study was not intended to clarify whether T3 affects vascular function through genomic or extranuclear mechanisms. However, the examination of the time course of FBF response to T3 infusion suggests that T3 acted through the activation of genomic mechanisms. This interpretation is also supported by the fact that by using the local infusion approach, the desired T3 concentration in the forearm is reached almost immediately, whereas the first demonstrable increment in FBF occurred after 2 h.

In a previous study in normal volunteers, T3 was able to reduce SVR as early as 3 min after the start of the infusion (29). This clearly speaks in favor of T3 ability to activate very rapidly nongenomic mechanisms. The data, however, are not in contrast with the present study, because we infused relatively low doses of T3, whereas in previous studies, T3 was used in big doses that raised the hormone concentration to more than 40 pg/ml (four times the values achieved in our study).

In conclusion, the present data demonstrate that T3 is a strong modulator of the resistance vessel response to vasoactive agents, as a consequence of an acute and direct interaction.


   Acknowledgments
 
We thank Dr. Emidio Botta, Dr. Michael Haring, and Henning GMBH, Sanofi-Synthelabo, Berlin, Germany, for the generous supply of Thyrotardin vials.


   Footnotes
 
This study was supported by a grant provided by the "Centro di Competenza GEAR" of Regione Campania.

Disclosure Summary: All the authors have nothing to declare.

First Published Online October 17, 2006

Abbreviations: Ach, Acetylcholine; FBF, forearm blood flow; fT3, free T3; FVR, forearm vascular resistance; L-NMMA, NG-monomethyl-L-arginine; NP, nitroprusside; SVR, systemic vascular resistance; TH, thyroid hormone; VSMC, vascular smooth muscle cell.

Received July 17, 2006.

Accepted October 10, 2006.


   References
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 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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