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J Am Dent Assoc, Vol 139, No 7, 940-946.
© 2008 American Dental Association
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RESEARCH

Burning Mouth Syndrome

An Evaluation of In Vivo Microcirculation



Giuseppe Alessandro Scardina, DDS, PhD, Teresa Pisano, DDS, Francesco Carini, MD, Vincenzo Valenza, MD and Pietro Messina, MD


   ABSTRACT
TOP
 ABSTRACT
SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background. Burning mouth syndrome (BMS) is an atypical orofacial algesic syndrome. The aim of the authors’ research was to investigate the morphological characteristics of peripheral blood circulation in patients with BMS in comparison with those of the peripheral blood circulation in healthy people.

Methods. The authors examined 28 subjects, of whom 14 (10 women and four men) had BMS and 14 (nine women and five men) were healthy control subjects. They performed videocapillaroscopic examination with a capillaroscope with a fiber-optic probe at a magnification of x200, which allowed them to examine the morphological characteristics within the capillaroscopic area accurately.

Results. The capillaroscopic examination provided important diagnostic results regarding alterations of the local microcirculation in subjects with BMS when compared with healthy subjects. The results also showed a statistically significant increase in the diameter of the capillary ansae, afferent ansae and efferent ansae in subjects with BMS compared with subjects in the control group (P = .05).

Conclusion and Clinical Implications. The results revealed a vascular involvement in BMS. This information could improve the understanding of etiopathogenetic factors and aid in the development of therapeutic strategies for treating this disorder.

Key Words: Burning mouth syndrome; mouth diseases

Abbreviations: BMS: Burning mouth syndrome • IL: Interleukin

Burning mouth syndrome (BMS) is a painful syndrome of which the frequency in the Italian population is significant. The syndrome affects 3.7 percent of the Italian population, and is more common in women (5.5 percent)—particularly after they experience menopause—than in men (1.6 percent).1 The prevalence of BMS in the world is about 8 percent.2

BMS often has an unknown etiopathogenesis and is associated with substantial clinical, diagnostic and therapeutic problems.3 It can be considered an atypical orofacial algesic syndrome owing to its clinical presentation.4,5 It is a clinical entity comprising various burning and dysesthetic conditions of the oral cavity that are not associated with visible alterations of the mucosa.6 Grushka and Sessle7 defined this condition as a burning sensation of the tongue and of other oral mucosa.

Because of the absence of a clear clinical objective assessment for this disorder and the lack of a definite understanding of its etiopathogenesis, the clinical interpretation and treatment of BMS remain problematic.8 A burning sensation is the pathognomonic symptom of BMS; it usually remains moderate but persists for long periods and therefore is difficult to tolerate. The pain is spontaneous and occurs without a triggering factor.1 The intensity of the pain varies among people, with patients reporting symptoms that range from mild to unbearable.9

Among the possible risk factors for BMS are numerous physiopathological situations in which the microcirculatory mechanisms are involved in pain generation. A local microcirculatory disturbance in the areas affected by BMS could contribute to the burning sensations described by patients. Some authors found that patients with BMS had parafunctional habits such as tooth grinding and clenching (bruxism) or tongue thrusting that could lead to changes in the intra-oral blood flow.10,11 The aim of our research was to study the morphology of the microcirculation in the affected areas in patients with BMS and compare it with that in equivalent areas in healthy people.


   SUBJECTS, MATERIALS AND METHODS
TOP
 ABSTRACT
 SUBJECTS, MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
We examined 28 subjects, 14 with BMS (10 women and four men, aged [mean ± standard deviation] 60.71 years ± 12.25) and 14 healthy people (nine women and five men, aged 60.42 years ± 14.21 [mean ± SD]), in our laboratory at the University of Palermo, Italy (Table 1Go). All patients signed a consent form as required by the Italian Ethical Committee. We excluded from the study smokers and subjects undergoing treatment with drugs that could alter microcirculation (such as antihypertensive, oral hypoglycemic or anti-inflammatory agents).


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  		TABLE 1 Demographic characteristics of the recruited subjects.

 
Neither the subjects with BMS nor the control subjects had any parafunctional habits that could alter microcirculation or produce inflammation in the oral mucosa. Subjects included in this study had a symptom typical of BMS: an extensive burning sensation in the oral cavity, particularly on the anterior one-third of the tongue.12 When diagnosing possible BMS, the clinician initially must exclude other pathologies that have similar symptoms.13–15 Therefore, we recommend that the clinician use oral swabs to obtain a fungal/bacterial microbiological culture, even if the painful areas of the oral mucosa have a normal appearance. Patients with BMS also may have allergies with or without oral manifestations (erythema). Thus, epicutaneous patch tests for both dental material and food allergens (such as nuts) are particularly indicated for patients whose medical history reveals evidence of hypersensitivity.16–20

In our study, we carried out the following assessments in our laboratory: microbiological culture assay (to rule out fungal infections), cutaneous allergy patch tests (to rule out food allergies), complete blood cell count, seric ferritin tests, vitamin B12 tests, glucose tests and salivary flow tests. We did not test for autoimmune conditions and thyroid dysfunction because they can influence microcirculation.21,22

The subjects with BMS had healthy oral mucosa, with all tests yielding negative results, leading to the diagnosis of BMS. The subjects with BMS were not under treatment for the condition.

We examined the subjects by using computerized videomicroscopic techniques and related software (Videocap 200, DS Medigroup, Milan, Italy). The optical probe videomicroscope is composed of a main unit, to which an optical probe with a video-optical terminal is connected, and a high-resolution color monitor to permit viewing of the examined area. The main unit consists of a 100-watt cold halogen light source with an incorporated electronic light intensity control and a processing unit for the high-definition video signal (420,000 pixels) with an incorporated color calibration device. The probe has a video-optical terminal containing a high-definition video sensor on which the user can apply different variable magnification optics from x10 to x1,000. One of the useful characteristics of the video-optical terminal is its ability to focus directly from the handpiece. Image digitization allows the user to analyze the fundamental parameters of the patient’s microcirculation (caliber and vessel length) and to calculate the number of capillaries per square millimeter of the mucosa. We used a lens with x200 magnification to identify the microangiotectonic type and group; this lens allowed us to explore accurately all of the morphostructural characteristics within the capillaroscopic area (a greater magnification does not allow proper focus on the capillary ansae).

One operator (G.A.S.) performed videocapillaroscopy on all subjects, who were in a seated position, by using the same light source at a constant room temperature (23°C) at the same time of day (morning); the operator performed the procedure twice in each investigated area (according to a method used in other studies23–26).

For each subject in both the BMS group and the control group, we observed the mucosa of the lower lip (frenulum), where the vascular bed is easily visible owing to the considerable thinness of the mucosal lining; the gingiva (sextant II); and the ventral surface of the tongue. In patients with BMS, all of the observed areas were affected by the condition.

One of the most important morphological parameters was the visibility of the ansae, which indicates the time taken by the instrument and its associated software to focus on the capillaries. In some portions of the mouth (the palate, for example), focusing on the vessels requires too much time, making it difficult for the patient to comply with the examination.26,27 We evaluated this parameter according to the following criteria:

– 1 = focusing easy (occurring within less than 30 seconds from the beginning of the examination);
– 2 = focusing relatively easy (occurring within 30 seconds to two minutes from the beginning of the examination);
– 3 = focusing difficult (occurring after more than two minutes from the beginning of the examination);
– 4 = focusing impossible.

Consecutively, we performed a morphofunctional evaluation of the microcirculation involving the following factors:

– length of the capillary ansae;
– diameter of the capillary ansae;
– afferent and efferent diameter;
– capillary density (the number of ansae per mm2);
– morphology of the ansae.

We examined and measured three capillary ansae per image, choosing the ansae on which the instrument could focus best (Table 2Go).


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  		TABLE 2 Evaluation of tortuosity and capillary ansae measurements in the lower lip.

 
We gave each ansa a tortuosity score from 0 to 3 on the basis of the number of crossings present: 0 = no crossings, 1 = one crossing, 2 = two or more crossings, 3 = distorted.

Statistical analysis. We used the Mann-Whitney test for nonparametric data to analyze the data gathered from the two groups (subjects with BMS and control subjects) to highlight any potentially significant statistical differences. This is considered to be one of the most efficient statistical tests, having 95 percent accuracy even when used to analyze numerically irrelevant samples.

We used a software called PAST (Version 1.81) to perform the data analysis. PAST is a freeware developed by Ø. Hammer, D.A.T. Harper and P.D. Ryan in 1995, last updated in April 2008.


   RESULTS
TOP
 ABSTRACT
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
We focused our investigation on the mucosa of the lower lip, the masticatory mucosa (gingivae) and the mucosa of the tongue. The capillaroscopy documented diversities in capillary location, shape and diameter, as well as in the microangiotectonic type, which is the general spatial distribution of the microcirculation, in the areas we observed.

In the mucosal lining of the lip, in subjects with BMS as well as in control subjects, the architecture of the microcirculation was compatible with Curri28 classification type I, group B (capillaries located parallel to the mucosal surface, with long capillary loops of even caliber and hairpin shape). In some cases, it was similar to Curri classification type III ("upturned U" or hairpin-shaped capillary ansae that form the classic "capillary comb"). The capillary ansae of the gingivae, on the other hand, had the typical characteristics of Curri28 classification type II, group A: the architecture of the microcirculation of the marginal gingiva did not show a constantly parallel orientation of the capillary loops in relation to the surface; only the apexes of the capillaries were visible; and the ansae had the aspect of evenly distributed dots or commas, resulting from a loop course perpendicular to the surface. Therefore, in this area we could observe only the density of the ansae. Owing to the dimensions of the probe, we did not examine the palate.

We examined the morphology of the ansae, which is one of the most important morphological parameters in BMS. Typically, the ansae were of a hairpin or comma shape, but we also observed some that were particularly curved and branched. This parameter is important because it is characteristic of the disorder. It is easy for an experienced observer to distinguish the morphology of ansae in patients with BMS from that of ansae in healthy people; therefore, evaluation of this parameter could lead to a preliminary diagnosis. (Such a diagnosis, however, always should be confirmed by further investigations.) In addition, we detected in subjects with BMS an altered capillary profile resulting from dilatations in the apical portion of the ansae.

The gravity and frequency of the morphofunctional alterations observed during the examination with the capillaroscope suggest a borderline result characterized by a slight alteration in the architecture of the microcirculation. We also observed a significant difference between the two groups in the diameter of the capillary ansae.

Some of the observed parameters varied in patients with BMS depending on the area under investigation but not depending on the intensity of the symptoms. In particular, we observed an increase in the total diameter of the capillary ansae, as well as a dilatation of the afferent and efferent ansae in patients with BMS. These alterations occured in both the lips and the tongue. In the gingival mucosa, we observed an increase in the capillary density in subjects with BMS, whereas we did not find this parameter’s result altered in the other two areas we examined.

Tables 3Go, 4Go and 5Go show the results of the statistical analysis. As Table 3Go and Figures 1Go, 2Go, 3Go (page 945) and 4 (page 945) show, the differences between the two groups in terms of total, afferent and efferent ansae diameters are significant.


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  		TABLE 3 Differences between parameters in the labial mucosa of subjects with BMS* and control subjects.{dagger}

 

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  		TABLE 4 Results of the statistical analysis performed with the Mann-Whitney test, regarding the masticatory mucosa alone.*

 

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  		TABLE 5 The differences between parameters in the tongues of subjects with BMS* and control subjects.{dagger}

 

Figure 1
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  		Figure 1. Labial microvascular characteristics in a subject with burning mouth syndrome (magnification x200).

 

Figure 2
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  		Figure 2. Labial microvascular characteristics in a healthy control subject (magnification x200).

 

Figure 3
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  		Figure 3. Lingual microvascular characteristics in a subject with burning mouth syndrome (magnification x200).

 

   DISCUSSION
TOP
 ABSTRACT
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
As far as we are aware, this is the first scientific study that has involved the use of videocapillaroscopy in the morphofunctional evaluation of microcirculation in subjects with BMS. The application of capillaroscopy led to important diagnostic results regarding the alterations of the local microcirculation in subjects with BMS when compared with that in healthy subjects.

Among the possible risk factors for BMS are numerous physiopathologic situations11,29–31 in which the circulatory mechanisms are involved in pain generation. A local circulatory disturbance of the areas affected by BMS could contribute to the burning sensations patients describe. Heckmann and colleagues10 investigated the mucosal blood flow in areas typically affected in patients with BMS. Their most interesting observations included a relative increase in vasoreactivity after application of dry ice in patients with BMS compared with that in healthy subjects and notably stronger reactions on the hard palate in patients with BMS than in subjects in the control group. They found no significant differences in the other areas they examined (the vestibule and the tongue). The stimulation with dry ice significantly altered the heart rate in both groups, and partial pressure of carbon dioxide did not differ between the two groups. Therefore, we can exclude these parameters as causes of the altered blood flow; consequently, these changes seem to be linked to the symptoms of BMS and imply a disturbed vasoreactivity in patients with this disorder.13

Other authors described a lower tongue temperature in patients with BMS, which also could indicate alterations of the autonomic functions.32 Still other researchers found parafunctional habits in patients with BMS, such as teeth grinding (bruxism) or habitual pressing of the tongue against the teeth, both of which could lead to changes in the intraoral blood flow.32–34

Our results point out that a disturbed regulation of the mucosal blood circulation plays a part in the symptoms of BMS. In other words, it seems that BMS results from, or affects, the neurovascular microcirculatory unit (that is, microcirculatory control of the sensory and autonomic innervation).

The capillaroscopic examination allowed us to detect a difference between subjects with BMS and healthy people in the diameters of the capillary, afferent and efferent ansae. In fact, the diameter of the ansae in subjects with BMS showed a statistically significant increase when compared with the diameter of the ansae in healthy mucosa (P = .05). Our research team has used capillaroscopy to investigate oral microcirculation in oral and systemic diseases; we observed oral microcirculatory alterations in patients with oral lichen planus or rheumatoid arthritis.35,36 In oral lichen planus, we found capillary density and diameters of the afferent and efferent ansae to be increased significantly.35,36 In patients who had rheumatoid arthritis, we observed a reduced caliber of the capillaries, as well as larger, elongated capillaries.

These results point toward the presence of a disturbance in the mucosal circulation, probably due to local inflammation.35,36 The vascular inflammation develops mainly in correspondence with the microcirculation in the periphery of the blood circulation.36 This process can be described as a sequence of the following events:

– vascular modifications of the micro-circulation, in particular variations in the vascular diameter and hematic flow;
– alterations of the blood-interstitial fluid exchange that leads to the formation of exudate;
– migration of leukocytes from the blood vessels toward the interstitial space.

These vascular modifications during vascular inflammation determine an active hyperemia, which is caused by an increase in the blood flow in the capillaries and is evident in the typical symptoms of calor and rubor. Active hyperemia can be brought on by different factors, such as an increase in the size of the circulatory bed, an increase in blood viscosity levels (caused mainly by aggregation of the red blood cells) or both, or the margination of the leukocytes that adhere to the endothelial wall.37

A study by Simcíc and colleagues38 showed an increase in the concentration of interleukin (IL)-6 and IL-2 in the saliva of subjects with BMS, which was correlated with the severity of their symptoms; the presence of these cytokines could explain the role of the inflammatory response in the etiopathogenesis of BMS. Pain is the principal symptom of the inflammation caused by local biochemical alterations. During the inflammatory process, important chemical mediators of plasmatic and cellular origin are produced; these have specific receptors, and a mediator can stimulate the release of other mediators by target cells with an amplifying, modulating or regulating effect. The mediators can act on one or many cellular types and have different effects depending on the type of tissue or cell; when they are produced or released, they have a short turnover. Inflammatory pain manifests as spontaneous pain and pain hypersensitivity. The spontaneous pain reflects the direct actions of specific receptors on free terminals of the nociceptors through inflammatory mediators.39


   CONCLUSION
TOP
 ABSTRACT
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
Although future research is necessary to enhance the findings of this study, the question remains whether the alterations we observed are a mere consequence of the symptoms of BMS or reflect a possible cause of the disorder. Furthermore, the presence of these alterations could be useful in establishing novel approaches to investigate therapeutic effects of drugs to combat this condition.26


Figure 4
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  		Figure 4. Lingual microvascular characteristics in a healthy control subject (magnification x200).

 


   FOOTNOTES
 

Dr. Scardina is a researcher, University of Palermo, Department of Oral Sciences "G. Messina," Via Del Vespro, 129-90127 Palermo, Italy, e-mail "scardina{at}odonto.unipa.it". Address reprint requests to Dr. Scardina.


Dr. Pisano is an internal dentist, Department of Oral Sciences, University of Palermo, Italy.


Dr. Carini is a researcher, Department of Experimental Medicine, University of Palermo, Italy.


Dr. Valenza is a professor, Department of Experimental Medicine, University of Palermo, Italy.


Dr. Messina is a professor, Department of Oral Sciences, University of Palermo, Italy.


Disclosure. None of the authors reported any disclosures.


   REFERENCES
TOP
 ABSTRACT
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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