Eur J Endocrinol
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DOI: 10.1530/eje.1.01903
European Journal of Endocrinology, Vol 152, Issue 4, 527-533
Copyright © 2005 by European Society of Endocrinology
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CLINICAL STUDY

Cardiac function in borderline hypothyroidism: a study by pulsed wave tissue Doppler imaging

Sandra Zoncu, Francesca Pigliaru1, Claudia Putzu1, Lorella Pisano, Sara Vargiu, Martino Deidda, Stefano Mariotti1 and Giuseppe Mercuro

Departments of Cardiovascular Sciences and 1 Endocrinology, Department of Medical Sciences, University of Cagliari, Sardinia, Italy

(Correspondence should be addressed to G Mercuro; Department of Cardiovascular Sciences, University of Cagliari, S.S. 554, bivio di Sestu, 09042 Monserrato, Cagliari, Italy; Email: mercuro{at}pacs.unica.it)


   Abstract
Top
 Abstract
Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Objective: In subclinical hypothyroidism (SH), impaired diastolic function has been documented at rest and on effort, while systolic dysfunction has only been assessed on effort.

Design: The aim of the present study was: (a) to further assess systolic function at rest in SH; and (b) to ascertain whether cardiac dysfunction could precede TSH increase in euthyroid patients with a high risk of developing SH.

Methods: We studied 32 patients with classical Hashimoto’s thyroiditis (22 with increased serum TSH (> 3 mU/ml – group A), and 10 with normal serum TSH (< 3 mU/ml – group B)); a third group (C), which included 13 healthy controls. All subjects underwent pulsed wave tissue Doppler imaging (PWTDI) to accurately quantify the global and regional left ventricular function.

Results: When compared with group C, PWTDI indices showed that in both groups A and B there was a significant impairment of systolic ejection (P < 0.001 and P < 0.05, respectively), a delay in diastolic relaxation (P < 0.001 and P < 0.05, respectively) and a decrease in the compliance to the ventricular filling (P < 0.05). Several significant correlations were found between PWTDI parameters and serum-free T3 and T4 and TSH concentrations.

Conclusion: PWTDI is a sensitive technique that allows detection of both diastolic and systolic abnormalities, not only in patients with SH, but also in euthyroid subjects with a high risk of developing thyroid failure. Futhermore, the significant correlations of several PWTDI indices with serum FT3 and TSH concentrations strongly support the concept of a continuum spectrum of a slight thyroid failure in autoimmune thyroiditis extending to subjects with serum TSH still within the normal range.


   Introduction
Top
 Abstract
 Introduction
Subjects and methods
 Results
 Discussion
 References
 
Subclinical hypothyroidism (SH) is a frequent condition defined by elevated thyroid stimulating hormone (TSH) secretion in the presence of normal concentrations of circulating thyroid hormones (1–3). Most cases of SH are due to the slow progression of thyroid failure caused by autoimmune thyroiditis and it is generally believed that the majority of patients with SH will eventually become frankly hypothyroid (2). Clinical symptoms and signs are often non-specific, and diagnosis and monitoring of therapy depend crucially on measurements of thyroid hormones and TSH in the blood (3–5). On the other hand, patients with unequivocal evidence of autoimmune thyroiditis may report symptoms (mainly chronic fatigue) even in the presence of normal serum TSH concentrations; the term ‘subchemical hypothyroidism’ has been suggested for this condition (6), but this remains open to speculation (7).

The clinical relevance of SH is still unclear, in spite of several reports of an increased risk of low density lipoprotein (LDL)-cholesterol and negative influence on the hemostatic profile, and of increased occurrence of coronary and peripheral arterial disease and depression (1–4). Several mild cardiac abnormalities, such as impairment of left ventricular diastolic function at rest and of systolic function on effort have been described in SH (8–12). These anomalies are probably responsible for a wide spectrum of symptoms suggestive of thyroid failure observed in patients with SH (13).

In the present study, taking advantage of the peculiar sensitivity of the heart to the action of the thyroid hormone, we assessed diastolic and systolic function in patients with SH and in subjects with euthyroid autoimmune thyroiditis with normal serum TSH concentration, but at risk of developing thyroid failure. For this purpose, we used pulsed wave tissue Doppler imaging (PWTDI), a technique based on the Doppler principle, which is able to precisely assess the ventricular wall motion (14).


   Subjects and methods
Top
 Abstract
 Introduction
 Subjects and methods
Results
 Discussion
 References
 
Study population

We studied 32 patients (31 females, one male) with documented classical Hashimoto’s thyroiditis (see below for the diagnostic criteria), whose main features are reported in Table 1Go. Twenty-two of them had SH with increased serum TSH (> 3 mU/ml: 5.40 ± 2.08 mU/ml, range 3.31–10.7 mU/ml; group A), and 10 had normal serum TSH (< 3 mU/ml: 2.27 ± 0.52 mU/ml, range 1.20–2.89 mU/ml; group B). Serum-free T3 (FT3) concentration was within the normal range in both groups. A third group included 13 healthy euthyroid controls (12 females, one male; group C). These were subjects who came to our laboratory for a thyroid function test and were found within normal values. All groups were matched for age, sex and body mass index (BMI) (Table 1Go). No significant differences were observed among the groups in heart rate, blood pressure and serum FT3 concentration. Mean serum-free T4 (FT4) concentration was significantly lower and mean serum TSH significantly higher in group A when compared with group B and C. Although individual serum TSH concentration in group B was within the normal range, its mean value was significantly higher in comparison with group C.


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  		Table 1 Biophysical characteristics, cardiovascular measurements and hormonal data of patients and controls.
 
Study protocol

The Ethical Committee of our University approved the present study, and informed written consent was obtained from all subjects. Participants were familiarized with instrumentation and medical environment of echocardiographic laboratory before testing. All subjects underwent physical examination, 12-lead electrocardiogram and M-mode, 2D and Doppler-echocardiography. Finally, subjects underwent PWTDI study, using an ultrasound system equipped with tissue Doppler imaging capabilities (SSA-380A; Toshiba Corp., Tochigi, Japan). A single experienced echocardiographer, who was unaware of the subjects’ thyroid conditions, carried out all examinations with subjects in the left lateral decubitus position. A simultaneous electrocardiographic tracing was also obtained.

Doppler echocardiography

A complete M-Mode, 2D, spectral- and color-Doppler recordings were performed using a 2.5-MHz transducer. Left ventricular mass (LVM) was measured according to the Devereux method (15); LVM index (LVMI) was obtained by dividing LVM by body surface area. Ejection fraction (EF) was calculated using the Simpson method (16). Pulsed Doppler transmitral flow velocities were recorded from the 4-chamber apical view, with the sample volume placed at the level of the mitral valve leaflet tips. Early (Em) and late (Am) diastolic velocities of transmitral flow were measured and the Em/Am ratio was derived. Isovolumic relaxation time (IVRT) was measured as the time interval between the end of systolic output flow and transmitral Em wave onset, by placing the sample volume between outflow tract and the mitral valve.

PWTDI

PWTDI uses the Doppler principle to assess the ventricular wall motion velocity by positioning the sample volume within the myocardium (14). In PWTDI, low-amplitude blood-flow signals are eliminated by gain adjustment to allow only high-amplitude Doppler signals from wall motion to enter the velocity calculation circuit. By means of a 4-chamber apical view, a 3 mm sample volume was placed both at the level of basal lateral and infero-septal mitral annulus, with the ultrasonic Doppler beam in a position as parallel as possible to the motion of the myocardial wall. Three distinct waves were obtained through PWTDI in each of the two mitral annular sites during the cardiac cycle: a systolic wave (S); an early diastolic wave (E) and a late diastolic wave (A). The following measurements were made from the PWTDI recordings: peak systolic velocity (Sa, cm/sec), acceleration time of S (ATSa, sec), deceleration time of S (DTSa, sec), peak early diastolic velocity (Ea, cm/sec), peak late diastolic velocity (Aa, cm/sec), acceleration time of E (ATEa, sec), and deceleration time of E (DTEa, sec). The Ea/Aa ratio was then calculated. Mean acceleration and deceleration rates of S (ARSa, cm/sec2; DRSa, cm/sec2) and of E (AREa, cm/sec2; DREa, cm/sec2) were obtained as Sa and Ea divided by their respective time intervals. These measurements were repeated on recordings of three consecutive cardiac cycles and their mean value was obtained. Then, values of basal lateral and infero-septal mitral annulus were averaged. Finally, we considered the peak early diastolic velocity of lateral mitral annulus (Eal, cm/sec) as a relaxation index. We then calculated the ratio between Em and Eal (Em/Eal), a parameter that takes into account the influence of cardiac relaxation on mitral flow (17). Reproducibility of PWTDI parameters in our laboratory had been previously documented (18).

Assessment of thyroid function

Serum TSH, FT4 and FT3, anti-thyroglobulin and anti-thyroid peroxidase antibodies (TgAb, TPOAb) were measured in all subjects. FT4 and FT3 were assayed by a direct method with chromatographic separation in Lisophase columns (Technogenetics, Milano, Italy). The normal ranges for FT4 and FT3 were 6.6–16 pg/ml and 2.8–5.6 pg/ml, respectively. Serum TSH was measured by immunochemiluminescent assay (Ortho-Clinical Diagnostic, Amersham, UK, normal range 0.3–3.0 mU/l). TPOAb were determined by RIA (ICN: normal range < 10 UI/ml); TgAb by passive hemoagglutination (Fujirebio Inc. Pharmaceuticals, Tokyo, Japan: normal range < 1/100). TPOAb ranged 64–3000 UI/ml (median 369) in group A, 134–3000 UI/ml (median 379) in group B, and were negative in controls. Thyroid ultrasound was performed in all cases using a 7.5 mHz linear electronic transducer, and thyroid echogenicity was subjectively evaluated by a conventional gray scale. The diagnosis of Hashimoto’s thyroiditis was made on the basis of hypoechoic goiter (19) associated to high levels of TPOAb and/or TgAb (20, 21).

Statistical analysis

Data from all groups are reported as mean ± S.D. Differences between control subjects and patients were assessed by the Student’s 2-tailed t-test for unpaired observations. Correlations between echocardiographic parameters and PWTDI indices, and hormones (FT3, FT4 and TSH) were evaluated using Pearson’s correlation coefficient. P values < 0.05 were considered to be significant.


   Results
Top
 Abstract
 Introduction
 Subjects and methods
 Results
Discussion
 References
 
Doppler echocardiography

In comparison with controls, Em and Em/Am ratio showed a significant decrease (P < 0.05 and P < 0.001, respectively), and IVRT a significant prolongation (P < 0.001) in group A (Table 2Go). Conversely, these parameters remained unmodified in group B. On the other hand, none of the echocardiographic parameters showed relevant differences between patients of group A and B. No single parameter of conventional echocardiography was correlated to serum TSH or FT3 concentration, with the exception of Em/Am ratio, which showed a significant inverse correlation (r = –0.36, P < 0.01) with serum TSH.


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  		Table 2 Left ventricle morphological and functional echocardiographic indices.
 
PWTDI systolic function

PWTDI systolic indices analysis revealed a significant impairment of the systolic ejection in both groups A and B, in comparison with group C, as shown by a decreased Sa and DRSa (P < 0.001 in group A, P < 0.05 in group B). Moreover, patients of group A showed an increase of TSa and DTSa (P < 0.05), and a decrease of ARSa and DRSa in respect to group C (P < 0.001). None of the systolic PWTDI indices showed significant differences between groups A and B. Table 3Go shows PWTDI systolic indices in all the groups.


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  		Table 3 Systolic mitral annulus indices assessed by PWTDI.
 
Table 4Go details correlations between PWTDI systolic indices and serum FT3, FT4 and TSH when patients of groups A, B and C were analyzed together. Taken collectively, the results showed significant correlations between most systolic indices and serum FT3 or TSH, whereas, with the exception of DRSa, no correlation was found with serum FT4. Some of these correlations are depicted in Fig. 1Go.


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  		Table 4 Correlations between PWTDI systolic indices and thyroid hormones in all subjects of Groups A, B and C.
 


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  		Figure 1 Selected correlations between plasma TSH concentrations and PWTDI systolic indices. {blacksquare} TSH > 3 mU/l patients (group A); {circ} TSH < 3 mU/l patients (group B); • control subjects (group C).

 
PWTDI diastolic function

PWTDI diastolic recordings analysis revealed a significant impairment of both diastolic relaxation (decreased Ea, AREa, DREa and Eal, P < 0.001) and compliance to the ventricular filling (decreased Ea/Aa ratio, P < 0.001, and increased Em/Eal ratio, P < 0.05) in groups A and B as compared with group C. None of the diastolic PWTDI indices showed significant differences between Groups A and B. Table 5Go displays PWTDI diastolic indices in all the three groups.


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  		Table 5 Diastolic mitral annulus indexes assessed by PWTDI.
 
Table 6Go shows correlations between PWTDI diastolic indices and serum FT3, FT4 and TSH when patients of groups A, B, and C were analyzed together. Again, in keeping with the important role of this hormone in determining cardiac function, most diastolic parameters were significantly associated to FT3. Surprisingly, three diastolic indices (Ea/Aa, Eal, Em/Eal) were strongly correlated to serum FT4 and TSH but not to serum FT3, thus suggesting a different sensitivity to circulating T3 and T4 concentrations. The correlations between serum TSH and selected PWTDI diastolic parameters are depicted in Fig. 2Go.


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  		Table 6 Correlations between PWTDI systolic indices and thyroid hormones in all subjects of Group A, B and C.
 


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  		Figure 2 Selected correlations between plasma TSH concentrations and PWTDI diastolic indices. {blacksquare} TSH > 3 mU/l patients (Group A); {circ} TSH < 3 mU/l patients (Group B); • control subjects (Group C).

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
References
 
In the present study we carried out an extensive investigation of cardiac function in patients with borderline or mild thyroid failure using PWTDI, a method of wall motion-velocity assessment for quantifying the dynamics of the cardiac cycle. The results obtained confirmed the presence of a diastolic dysfunction in patients with SH and provided further evidence that an impairment of systolic function is present in mild thyroid failure, and also at rest. Moreover, our results provided the first evidence that a subtle impairment in both systolic and diastolic function is also detected in patients with autoimmune thyroiditis with serum TSH concentration still comprised within the normal range.

As far as the diastolic function is concerned, our results with PWTDI are in keeping with several previous studies (for extensive reviews see (10, 11)) carried out by conventional echocardiography, documenting the presence of a significant diastolic impairment in patients with SH. With respect to conventional echocardiography, PWTDI allowed the use of Eal, a relaxation index independent from the preload, and of Em/Eal, a filling index closely correlated with the wedge pressure (17). This approach avoided the potential confounding effects of conventional echocardiography indices of left ventricular filling assessed by Doppler transmitral flow, e.g. Em/Am, which are influenced by several confounding factors such as age, heart rate, preload and afterload (22).

In contrast with the consistent findings on diastolic function, the literature provided conflicting data on systolic function in patients with SH. Biondi et al. (8) reported a significant reduction of the mean aortic acceleration, whereas peak aortic flow velocity, cardiac output, fractional shortening, and mean velocity of circumferential fiber shortening remained unaltered (8). An impairment of systolic function was observed by means of the systolic time interval, which shows the limits of an indirect method, inferred by the integration of electrocardiographic and Doppler data (9, 12). Systolic abnormalities were detected with certainty in SH only in the course of physical exercise, when the evaluation of the cardiac performance is favored by the discrepancy between the energy request and the functional cardiac reserve (8, 9, 12). In this context, SH has been found to be associated with a deranged cardio-respiratory function, both at the level of anaerobic threshold and at peak exercise (23). Evidence suggesting systolic abnormalities in SH has recently been reported by other techniques such as ultrasonic myocardial textural analysis (24), impedance cardiography (25), and radionuclide ventriculography (26).

By means of recordings performed at several sites of the mitral annulus, the PWTDI technique produces an average figure of the structure displacement velocity, which represents a reliable index of global systolic function (27). This methodological approach allowed us to demonstrate that an impairment of the systolic phase is also present at rest in patients with SH.

On account of the assumption that PWTDI is the most sensitive technique to assess the effects of subtle thyroid failure on heart contractility, we decided to use it to test the possibility that patients with autoimmune thyroiditis and normal TSH levels (i.e. those with a high risk of developing SH or overt thyroid failure) may actually be slightly hypothyroid: this condition has been recently envisaged (6, 28) but, to our knowledge, no investigation (and particularly no studies on heart contractility) has been carried out to directly address the question.

Unlike conventional echocardiography, which did not show any significant alteration in both systolic and diastolic function of patients with ‘euthyroid’ autoimmune thyroiditis, PWTDI allowed us to detect a subtle but significant impairment in the whole cardiac function of these individuals. In detail, our findings were consistent in showing a significant impairment of left ventricular ejection (decreased Sa and DRSa), diastolic relaxation (decreased Ea, AREa, DREa and Eal) and ventricular filling (decreased Ea/Aa ratio and increased Em/Eal).

The degree of derangement of the above parameters found in patients with ‘euthyroid’ autoimmune thyroiditis was always intermediate between patients with SH and normal euthyroid controls.

These results, along with the significant correlations of a number of PWTDI indices with thyroid hormones and TSH concentrations, strongly support the concept of a continuum spectrum of a slight thyroid failure in autoimmune thyroiditis extending to subjects with serum TSH still within the normal range. The majority of PWTDI indices were correlated to serum FT3 rather than FT4 concentrations. This proves the pivotal role of T3 in cardiac function. Moreover, some diastolic indices such as Ea/Aa, Eal and Em/Eal were significantly correlated to FT4 but not to FT3. The reason for such findings is unclear and cannot be derived from the present data. We are inclined to think that some indices may be more affected by local generation of T3 (from circulating T4) than by circulating T3. Indeed, autoimmune thyroid disease is so common in the population (up to 40% of women with lymphocytic infiltration of the thyroid and 10–15% with thyroid autoantibodies) (1–4), that laboratory reference ranges derived from apparently healthy subjects could easily be affected by diseased individuals. In keeping with this concept, increased prevalence of TPOAb has been found in subjects with serum TSH concentrations outside the narrow range 0.2–1.9 mU/l, providing evidence that TSH in the upper reference range is often associated with abnormal pathology in the thyroid (7).

In conclusion, by showing an impaired systolic function in the basal condition of patients with SH, the tissue Doppler imaging has extended our knowledge of the cardiac involvement in this disease. However, the clinical relevance of this finding and the effects of L-thyroxine substitution therapy remain matters for further investigation.


   Acknowledgements
 
The authors thank Enrico Lampis, MA, for his technical assistance in preparing the manuscript.


   References
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

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Received 21 January 2005
Accepted 4 February 2005




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