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International Journal of Morphology

versión On-line ISSN 0717-9502

Int. J. Morphol. v.25 n.2 Temuco jun. 2007 


Int J. MorphoL, 25(2):411-416,2007.


Hashimoto's Thyroiditis: Lingual and Labial Capillary Microcirculation in Patients Affected by Macroglossia

Tiroiditis de Hashimoto: Microcirculación Lingual y Labial en Pacientes Afectados por Macroglosia


Scardina G. A. & Messina P.

Department of Oral Science-University of Palermo-Italy.

Dirección para correspondencia

SUMMARY: The aim of this study is to estudy lingual and labial microcirculation differences among healthy subjects and those with Hashimoto's thyroiditis affected by macroglossia. Twenty healthy patients and 20 patients suffering from Hashimoto's thyroiditis were examined. Labial and lingual capiUaroscopy were used to investigate the characteristics of microcirculation. For each patient we evaluated visibility, course, tortuosity and the possible presence of microhaemorrhages, average calibre of capillary loops and the number of visible capillary loops per square millimetre. The investigations of the labial and lingual mucous were simple, non invasive and repeatable for each patient. In Hashimoto's thyroiditis patients it was possible to observe a wide vascular architectural disorganisation, morphologic anomalies of the capillary loops, loosening of the U shape, reduced capillary diameter This study shows that capillary alterations in patients suffering from Hashimoto's thyroiditis occur in the labial and lingual mucous microcirculation. In the patients affected by macroglossia a reduced number of capillary density was observed and it was correlated to the deposition of proteinaceous ground substance.

KEYWORDS: Oral capiUaroscopy; Hashimoto's thyroiditis; Macroglossia.

RESUMEN: El objetivo de este estudio fue verificar las diferencias en la microcirculación lingual y labial entre sujetos sanos y con tiroiditis de Hashimoto afectados por macroglosia. Fueron examinados 20 pacientes sanos y 20 que sufrían de tiroiditis de Hashimoto. Fue utilizada capiloroscopía labial y lingual para investigar las características de la microcirculación. Para cada paciente examinamos visibilidad, curso, tortuosidad y la posible presencia de microhemorragias, el calibre medio de curvaturas capilares y el número visible de curvaturas capilares por milímetro cuadrado. La investigación de la mucosa labial y lingual fue simple, no invasiva y repetible para cada paciente.

En pacientes con tiroiditis de Hashimoto fue posible observar una desorganización arquitectónica vascular, anomalías morfológicas de las curvaturas capilares, pérdida de la forma de U y reducción del diámetro capilar. Este estudio demuestra que las alteraciones capilares en pacientes que sufren de tiroiditis de Hashimoto ocurren en la microcirculación de la mucosa labial y lingual. En los pacientes afectados por macroglosia fue observada una reducción de la densidad capilar y esto está correlacionado a la deposición de

PALABRAS CLAVE: Microscopía oral; Tiroiditis de Hashimoto; Macroglosia


Primary hypothyroidism, the most common form, is an autoimmune disease, usually occurring as a result of Hashimoto's thyroiditis and is associated often with a firm goiter or, later in the disease process, with a shrunken fibrotic thyroid gland with little or no function (Lorini et al., 2006 Okamoto, 2006).

The symptoms of primary hypothyroidism are: the facial expression is dull; the voice is hoarse and speek is slow; cold intollerance may be prominent; hair is sparse, coarse, and dry. Weight gain is modest and is largely the result of decreased metabolism of food and fluid retention. Patients are forgetful and show other evidence of intellectual impairment, with a gradual change in personality. Some appear depressed ( Syrenicz et al., 2005; Volpe, 1981).

The aim of this study is to observe lingual and labial microcirculation in patients suffering from Hashimoto's thyroiditis.


Twenty healthy subjects (8 males and 12 females; mean±SD age: 26.2+1.9 years; range: 18-42 years) and 20 patients with Hashimoto's thyroiditis (8 males and 12 females; mean±SD age: 24.6+1.2 years; range: 18-44 years) were examined in our laboratory.

Healthy subjects were included in the study only if the accurate exam of their medical history and the objective examination of their oral mucosa revealed that they were non smokers.

All subjects provided informed consent for the processing and use of their personal medical data in scientific papers, according to the Italian law.

The patients were examined by computerised videomicroscopic techniques and related software (Videocap 200-DS medigroup MI).

The capillaroscopic investigation was carried out with the patients in a sitting position, with the same light source, at the same room temperature (23°C), in the morning, by the same operator and repeated twice for each examined area.

The examined area was always the same for each patient: - the fraenum area of the lower lip and left margin of the tongue.

Two independent observers examined all the images. The intraobserver and interobserver variability was assessed with the two observers evaluating twice the same randomly selected images.

The following static parameters were used:

A) Nonparametric data: capillary loop visibility (score from 1 to 4): 1) simple focusing - within 30 seconds from the beginning of the examination; 2) average focusing - over 30 seconds and within 2 minutes; 3) difficult focusing - over 2 minutes; 4) impossible focusing; orientation regarding the surface (score A, B or AB): A) capillary loop course parallel to the surface;

B) capillary loop course perpendicular to the surface; AB) both parallel and perpendicular; capillary tortuosity (score from 0 to 3): 0) absence of crossing in the capillary loops; 1) presence of crossing; 2) greater presence of crossing; 3) complete distortion of the capillary loops; microhaemorrhages (score 0 or 1): 0) absence; 1) presence; characteristics of the capillary loops (score 0 or 1): 0) absence; 1) presence.

B) Parametric data: number of visible capillary loops in every square millimetre (value obtained from the average of the two observations for each examined area); capillary loop calibre (values obtained from the average of the two observations for each examined area).

All patients involved in the study kept a dietary diary for a period of three months, in order to evaluate any dietary differences possibly affecting the oral capillary pattern observed.

The preferred test was the Mann-Whitney U test for ordinal, non-parametric data.

The computer support used was P.A.S.T. software v. 1.53, a freeware software developed in 1995 by P.D. Ryan, D.A.T. Harper and J.S. Whalley, updated to the latest version in September 2006. The results of the statistical analysis of the data, divided according to the parameters, are reported below.

The graphical representation (Charts 1 and 2) of what has been described above is of great visual impact, and clearly shows how the collected data of the two groups are significantly different.

The results obtained from each examined area represent the average values of the two observations.


Intrasubject variability satisfied the priori hypothesis of a limited dispersion. For the parametric data, variability ranged from +2% to -2% regarding the mean value. For the non-parametric data, 1 score point difference at most was observed.

No significant differences were detected between healthy and Hashimoto's thyroiditis subjects in age (P>0.01, MWtest).

Labial microcirculation: The visibility of the microcirculation was simple in both patient and control group.

The microcirculation architecture in healthy subjects was characterised by a network of capillaries in polygonal mesh and a parallel orientation (type A) regarding the surface. The microcirculation architecture in Hashimoto's thyroiditis patients was characterised by an anarchical arrangement of the capillary major axis.

The tortuosity of the capillaries in healthy subjects showed a score=0 in 15 patients; score=l in 5 patients. In patients with Hashimoto's thyroiditis, capillaries tortuosity showed score=0 in 1 patient; score= 1 in 4 patients; score=2 in 4 patients; score 3 in 11 patients (p<.001). Rare microhemorrhages (score=l) were observed in 2 healthy patients. These were identified as reddish stains, that could have been caused by possible microtraumas. No microhemorrhages were observed in Hashimoto's thyroiditis patients.

The calibre of the visible capillary loops was 18.92+2.4 µm (mean+SD) in healthy subjects and 6.4+1.2 µm (mean+SD) in patients with Hashimoto's thyroiditis (P<.001,MW test). The number of capillaries visible was 8.44+1.68 (mean+SD) in healthy subjects and 7.9+1.1 (mean+SD) in patients with Hashimoto's thyroiditis (P>.001, MWtest). Fig. 1.

No significant differences in the alimentary habits of patients were detected.

The results of the labial observations are summarised in Table I.

Lingual microcirculation.The visibility of the microcirculation was simple.

The microcirculation architecture in Hashimoto's thyroiditis patients was characterised by an anarchical arrangement of the capillary major axis.

In patients with Hashimoto's thyroiditis, capillaries tortuosity showed score=0 in 2 patient; score= 1 in 6 patients; score=2 in 4 patients; score 3 in 8 patients (p<.001).

The calibre of the visible capillary loops was 16.94+1.7 µm(mean+SD) in healthy subjects and 7.4+1.9 µm (mean+SD) in patients with Hashimoto's thyroiditis (P<.001,MW test). The number of capillaries visible was 7.35+1.48 (mean+SD) in healthy subjects and 4.1 + 1 (mean+SD) in patients with Hashimoto's thyroiditis (P<001, MW test) Table III.


The authors observe "in vivo" the microvascular characteristics of the labial and lingual mucosa in Hashimoto's thyroiditis patients affected by macroglossia.

The investigation method appear quite simple, immediate and permits the extrapolation of parametric and non-parametric data (Cantatore et al.,2000;Cinti et al., 1984;Curri, 1992; Del Guercio & Piovella, 1995; Grassi et al, 1984a, b).

Capillaroscopy is a non-invasive diagnostic technique, fundamental in viewing peripheral circulation and in studying microangiopathies, which are the manifestations of numerous pathologies in both the diagnostic and monitoring phases of the disease.

Affected capillaries are characterized by distorted and irregular loops. The capillary density was reduced corresponding to the lingual microcirculation. We think that this was correlated to the deposition of proteinaceous ground substance and consequent macroglssia. The value of capillaroscopic investigation as a diagnostic means for peripheral microcirculation damage is confirmed by numerous studies (Haak et al, 1998; Halfoun et al, 2003).

Our study shows that capillaroscopy is a reliable method for studying labial and lingual microcirculation. The advantages of oral mucous as a capillaroscopic examination area, result in a satisfying evaluation of microcirculation for the excellent mucous transparency, especially at the labial level; in an easily approachable exam area; in the lack of local mechanical or chemical microcirculation stimulation, and in a reduced susceptibility to the "cold stress" due to the contact ofthe mucous to the probe (Mahler et al., 1987; Miniati et al., 2001; Scardina et al, 2004; Scardina & Messina, 2004). This study demonstrates that capillaroscopic alterations during Hashimoto's thyroiditis result in the oral mucous peripheral circulation.

Labial capillaroscopy in patients with Hashimoto's thyroiditis revealed significant microvascular changes regarding the controls.

Lingual and capillaroscopic pattern in patients with Hashimoto's thyroiditis is recognisable by a direct evaluation and is characterised by:

-  wide architectural disorganisation;
-  loosening ofthe U shape capillaries with a high degree of heterogeneity in shapes characterised by reduced calibre;
- reduced capillary density corresponding to lingual microcirculation.

This study shows that capillary alterations in patients suffering from Hashimoto's thyroiditis occur in the oral microcirculation.



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Received: 18-12-2006 Accepted: 22-03-2007

Correspondence to:

Dr. Scardina Giuseppe Alessandro
University of Palermo
Department of Oral Science "G.Messina"
via Del vespro,129 90127
Palermo - ITALIA



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