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https://doi.org/10.15644/asc50/2/8

Dorsal Lingual Surface and Halitosis: a Morphological Point of View

Sara Bernardi   ORCID icon orcid.org/0000-0001-6130-8533 ; Department of Life, Health & Environmental Sciences, University of L’Aquila, Italy
Giuseppe Marzo ; Department of Life, Health & Environmental Sciences, University of L’Aquila, Italy
Maria Adelaide Continenza ; Department of Life, Health & Environmental Sciences, University of L’Aquila, Italy

Puni tekst: engleski, pdf (620 KB) str. 151-157 preuzimanja: 195* citiraj
APA 6th Edition
Bernardi, S., Marzo, G. i Continenza, M.A. (2016). Dorsal Lingual Surface and Halitosis: a Morphological Point of View. Acta stomatologica Croatica, 50 (2), 151-157. https://doi.org/10.15644/asc50/2/8
MLA 8th Edition
Bernardi, Sara, et al. "Dorsal Lingual Surface and Halitosis: a Morphological Point of View." Acta stomatologica Croatica, vol. 50, br. 2, 2016, str. 151-157. https://doi.org/10.15644/asc50/2/8. Citirano 19.09.2020.
Chicago 17th Edition
Bernardi, Sara, Giuseppe Marzo i Maria Adelaide Continenza. "Dorsal Lingual Surface and Halitosis: a Morphological Point of View." Acta stomatologica Croatica 50, br. 2 (2016): 151-157. https://doi.org/10.15644/asc50/2/8
Harvard
Bernardi, S., Marzo, G., i Continenza, M.A. (2016). 'Dorsal Lingual Surface and Halitosis: a Morphological Point of View', Acta stomatologica Croatica, 50(2), str. 151-157. https://doi.org/10.15644/asc50/2/8
Vancouver
Bernardi S, Marzo G, Continenza MA. Dorsal Lingual Surface and Halitosis: a Morphological Point of View. Acta stomatologica Croatica [Internet]. 2016 [pristupljeno 19.09.2020.];50(2):151-157. https://doi.org/10.15644/asc50/2/8
IEEE
S. Bernardi, G. Marzo i M.A. Continenza, "Dorsal Lingual Surface and Halitosis: a Morphological Point of View", Acta stomatologica Croatica, vol.50, br. 2, str. 151-157, 2016. [Online]. https://doi.org/10.15644/asc50/2/8
Puni tekst: hrvatski, pdf (620 KB) str. 151-157 preuzimanja: 111* citiraj
APA 6th Edition
Bernardi, S., Marzo, G. i Continenza, M.A. (2016). Dorzalna površina jezika i halitoza: morfološki aspekti. Acta stomatologica Croatica, 50 (2), 151-157. https://doi.org/10.15644/asc50/2/8
MLA 8th Edition
Bernardi, Sara, et al. "Dorzalna površina jezika i halitoza: morfološki aspekti." Acta stomatologica Croatica, vol. 50, br. 2, 2016, str. 151-157. https://doi.org/10.15644/asc50/2/8. Citirano 19.09.2020.
Chicago 17th Edition
Bernardi, Sara, Giuseppe Marzo i Maria Adelaide Continenza. "Dorzalna površina jezika i halitoza: morfološki aspekti." Acta stomatologica Croatica 50, br. 2 (2016): 151-157. https://doi.org/10.15644/asc50/2/8
Harvard
Bernardi, S., Marzo, G., i Continenza, M.A. (2016). 'Dorzalna površina jezika i halitoza: morfološki aspekti', Acta stomatologica Croatica, 50(2), str. 151-157. https://doi.org/10.15644/asc50/2/8
Vancouver
Bernardi S, Marzo G, Continenza MA. Dorzalna površina jezika i halitoza: morfološki aspekti. Acta stomatologica Croatica [Internet]. 2016 [pristupljeno 19.09.2020.];50(2):151-157. https://doi.org/10.15644/asc50/2/8
IEEE
S. Bernardi, G. Marzo i M.A. Continenza, "Dorzalna površina jezika i halitoza: morfološki aspekti", Acta stomatologica Croatica, vol.50, br. 2, str. 151-157, 2016. [Online]. https://doi.org/10.15644/asc50/2/8

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Sažetak
Objective: The interest in the study of the tongue papillary niches and the related biofilm has increased in recent years because they form a suitable source of periodontal microorganisms and are associated with development of halitosis. Tongue dorsum structure represents a factor favoring a particular and complex bacterial biofilm where periodontal pathogens are frequently found. The aim of this preliminary study was to associate the tongue papillary structure with the biofilm causing halitosis by means of a new clinical protocol. Material and Methods: In this study, one subject affected by oral malodor was selected and included. A photograph of lingual dorsum was taken to spot the areas with visible lingual coating. A tongue dorsum impression was obtained, divided and cut with a blade in six parts, according to Winkel Tongue Coated Index by means of the 2-step double-mix impression technique. The contours of the six parts were observed by the stereomicroscope LEICA LED2000 and analyzed by ImageJ software. Results : The results showed that the depth of papillae was associated with visible presence of the tongue biofilm and indirectly correlated with halitosis in patients.. Conclusions: The morphological papillary structure of the tongue dorsal surface influences the presence of the tongue biofilm. The presented protocol can be further considered in clinical application for a correct diagnosis and a personalized treatment of halitosis.

Ključne riječi
Halitosis; Tongue; Bacterial Adhesion; Winkel Tongue Coated Index; Clinical Protocols

Hrčak ID: 160307

URI
https://hrcak.srce.hr/160307

▼ Article Information



Introduction

The usual appearance of the dorsal surface of the tongue is either pinkish or with a thin white coating. This surface is colonized by large amounts of bacteria, mostly in the presence of fissures, crypts and high mucosal papillae. These anatomical niches create an environmental condition where microorganisms are embedded and well-protected from the flushing action of the saliva. Also, oxygen levels in such environment are low, thus promoting the development of anaerobic microbiota (1). The coating of the tongue consists of a visible white-brownish layer adhering to the dorsum of the tongue and embedding desquamated epithelial cells, blood cells and metabolites, nutrients and bacteria. Indeed, more than 100 bacterial species were found attached to a single epithelial cell on the dorsum of the tongue, whereas only about 25 bacteria adhere to each cell in other areas of the oral cavity (2). Different indexes were developed for quantifying the degree of tongue coating: Miyazaki et al. (3) reported that tongue coating is present or absent in three areas, while no indication of thickness was recorded. Winkel at al. (4) divided the tongue in six areas, scoring each one independently from 0 (no coating) to 1 (light coating) and 2 (heavy coating). The final value of the Winkel Tongue Coating Index has been obtained by adding all six scores. Therefore, the tongue microflora offering a large surface area represents a unique ecological niche in the oral cavity. The dorso-posterior surface of the tongue was reported to harbor a high quantity of attached microbes (109 or 1010 CFU cm2) (5). Oral malodor is a common problem affecting a large percentage of the adult population (6, 7) and volatile sulfur compounds (VSC) are thought to be the most important volatile components.

The tongue biofilm is considered to be the principle site for the generation of VSC accounting for 60–70% of the total, with plaque contributing the rest (2, 8).

The studies show that bacteria residing on the tongue make the dominant contribution to oral malodor (9, 10).

The surface of the tongue has been described by Maeda (11) as a surface consisting of papillae oriented perpendicular to the tongue plane. Hesse modelled a three dimensional structure of the substratum and biofilm with the first layer consisting of the connective tissue core of the papillae, the second layer having a thin biofilm cover and the last one consisting of a thick biofilm cover. The uppermost layer of the biofilm is considered to be aerated and hence aerobic, whereas deeper layers of the biofilm are anaerobic (12). Hesse (13) reported that in case the forces are applied to the papillae, for example, when scraping the tongue, the papillae bend slightly and protect the biofilm, thus remaining in the interstitial volume. This demonstrates the significant influence of the substratum structure on the stability of the tongue biofilm under mechanical stress. Each papilla itself cannot be seen just as a simple stud sticking out from the surface of the tongue but a cluster of individual strands, as showed by Kobayashi et al. (14). The presence of deep fissures has been related to twice the total counts of bacteria and to significantly higher mouth and tongue odor scores (15), although other authors have failed to confirm the association of higher bacterial counts with increased surface roughness of the tongue (16, 17).

The aim of this research was to correlate the roughness of the tongue with the presence of the tongue coating biofilm in a halitosis patient. A preliminary protocol was designed for this purpose.

Material and Methods

One subject with halitosis was selected and included in the study. A picture of the lingual dorsum was taken to spot the areas where the coating was visible (Figure 1).

Figure 1 the tongue with visible biofilm
ASC_50(2)_151-157-f1

The first impression was taken by alginate obtaining an exact replica in plaster and an impression tray was modelled utilizing silicone putty impression material. Subsequently, the second impression was taken combining the tray in silicone putty with a silicone material, thus having a very low-light density (using the 2-step double-mix impression technique) (Figures 2-3).

Figure 2 the plaster model
ASC_50(2)_151-157-f2
Figure 3 2-step double-mix impression
ASC_50(2)_151-157-f3

The obtained impression was divided and cut with a blade in six parts, according to Winkel Tongue Coated Index (18), and their contours were observed with the stereo-microscope LEICA LED2000. The images were analyzed by the Image J software (19), and the depths among papillae were considered to be parameters.

The obtained data were processed by descriptive statistical analysis (Mean, SD, Shapiro-Wilk Normality, and T-Student) using the XLSTAT software (2015.4.01. version).

Results

The stereomicroscope observation revealed some interesting outcomes. The parameter considered was the depth of the fissures on the long and on the short side of each zone (Figures 4-5), and such mean values were compared between the 6 zones. The 6 zones were divided in two groups, based on the visibility of the biofilm on the taken picture.

Figure 4 Impression cut according to the Winkel Index Coating
ASC_50(2)_151-157-f4
Figure 5 Stereomicroscope pictures at 2X magnification
ASC_50(2)_151-157-f5

All of the six zones resulted by following a normal distribution (Figures 6).

Figure 6 Normality test P-P plot: the spot under the diagonal line shows a normal distribution
ASC_50(2)_151-157-f6

The zones A, B and C mean values resulted respectively as 0.25 + 0.05 mm, 0.46 + 0.23 mm and 0.17 + 0.03 mm. These three zones produced those with high visible presence of biofilm on the taken picture.

The zones D, E and F mean values resulted respectively as 0.20 + 0.07 mm, 0.28 + 0.12 mm and 0.14 + 0.05 mm. These three zones produced those with a low visible presence of biofilm on the taken picture. The first group (A-B-C) showed higher values of depth fissures compared to the second group (D-E-F). The difference between the two groups was statistically significant with a p value < 0.05 (Tables 1-2).

Table 1 Shapiro-Wilk Normality test
ZONEMean Value (mm)SDShapiro-Wilk Normality test (P value)
Zone A0.250.05> 0 .05
Zone B0.460.23> 0 .05
Zone C0.170.03> 0 .05
Zone D0.200.07> 0 .05
Zone E0.280.12> 0 .05
Zone F0.140.05> 0 .05
Table 2 Shapiro-Wilk Normality test
High visible presence of biofilm (A-B-C) mean values mmLow visible presence of biofilm (D-E-F) mean values mmP value *
0.3 + 0.180.21 + 0.1< 0.05

*T-Student test

Discussion

The papillary structure of the dorsum represents a unique ecological niche in the oral cavity, offering a large surface area that favors the accumulation of oral debris and microorganisms. In addition, its location as a crossroad between the oral cavity and the pharynges provides access to many different types of nutrients, products and bacteria (20).

It is a well-known fact that dorsal surface of the human tongue includes four distinct types of papillae: filiform, distributed over the dorsum; fungiform, located anteriorly; foliate found in the lateral posterior regions and circumvallate located along the sulcus (21).

The dorsal surface of the tongue is described as a set of various papillae and taste buds. Each papilla itself can be seen as a cluster embedded in a matrix, and the saliva, which in turn is exposed to the mouth gaseous air. This implies a particular oxygenation of the biofilm that is created on this surface: the oxygen level is very low in deep surfaces of the papilla and it is consumed by the metabolisms of the bacteria. Conversely, the level of oxygen is higher at the top of the surface (13).

This structure and its ecological layout favors the harbor of different species of bacteria, and its roughness allows the adhesion and the formation of a biofilm where the bacteria coexist (22).

The surface roughness degree can change due to several factors including age, sex salivary secretion, immunological defense, gastrointestinal disorders (21).

An atrophic tongue can be caused by nutritional deficiencies, as well as candidiasis or by Sjogren syndrome (23) (24).

Murayama and Kobayashi reported that the protrusions of filiform papillae and taste pores of fungiform papillae were successfully reproduced by using a low viscous silicone impression material (25).

In 2012, Uemori et al. carried out a study on reliability of the tongue impression in order to determine the roughness of the tongue dorsum and to exploit it as diagnostic tool to quantify the degree of atrophy as well as morphology of the lingual papillae (26).

The results obtained in the present study reveal that the depths of papillae and fissures were expressed quantitatively. Also, the relationship between the coated biofilm found in a halitosis-affected subject and the abovementioned depths was analyzed. The method used in this study appeared to be correct, as confirmed by the cited authors. It allowed us to investigate morphologically the papillary structure and to associate it with a visible biofilm presence.

Our study confirmed the fact that the tongue dorsum morphology offers a unique environmental niche for biofilm coating and adhesion. Thus, the study of its roughness and its papillary structure is fundamental for diagnosis and personalized treatments of pathologies affecting this organ.

Notes

[1] Conflicts of interest Authors declare they have no conflict of interest.

Acknowledgement

Preliminary data regarding this study were presented as poster at the 67th National Congress of Italian Society of Anatomy and Histology

References

1 

Roldán S, Herrera D, Sanz M. Biofilms and the tongue: therapeutical approaches for the control of halitosis. Clin Oral Investig. 2003 Dec;7(4):189–97. DOI: http://dx.doi.org/10.1007/s00784-003-0214-7 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/14513303

2 

Yaegaki K, Coil JM. Examination, classification, and treatment of halitosis; clinical perspectives. J Can Dent Assoc. 2000 May;66(5):257–61. PubMed: http://www.ncbi.nlm.nih.gov/pubmed/10833869

3 

Miyazaki H, Sakao S, Katoh Y, Takehara T. Correlation between volatile sulphur compounds and certain oral health measurements in the general population. J Periodontol. 1995 Aug;66(8):679–84. DOI: http://dx.doi.org/10.1902/jop.1995.66.8.679 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/7473010

4 

Roldán S, Winkel EG, Herrera D, Sanz M, Van Winkelhoff AJ. The effects of a new mouthrinse containing chlorhexidine, cetylpyridinium chloride and zinc lactate on the microflora of oral halitosis patients: a dual-centre, double-blind placebo-controlled study. J Clin Periodontol. 2003 May;30(5):427–34. DOI: http://dx.doi.org/10.1034/j.1600-051X.2003.20004.x PubMed: http://www.ncbi.nlm.nih.gov/pubmed/12716335

5 

Hartley MG, El-Maaytah M, McKenzie C, Greenman J. The Tongue Microbiota of Low Odour and Malodorous Individuals. Microb Ecol Health Dis. 1996 Nov;9(5):215–23. DOI: http://dx.doi.org/10.3109/08910609609166462

6 

Tonzetich J. Production and origin of oral malodor: a review of mechanisms and methods of analysis. J Periodontol. 1977 Jan;48(1):13–20. DOI: http://dx.doi.org/10.1902/jop.1977.48.1.13 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/264535

7 

Tonzetich J. Oral malodour: an indicator of health status and oral cleanliness. Int Dent J. 1978 Sep;28(3):309–19. PubMed: http://www.ncbi.nlm.nih.gov/pubmed/279515

8 

Sterer N, Rosenberg M. Breath Odors: Origin, Diagnosis, and Management. Springer Science & Business Media; 2011. 125 p.

9 

Gerlach RW, Hyde JD, Poore CL, Stevens DP, Witt JJ. Breath Effects of Three Marketed Dentifrices: A Comparative Study Evaluating Single and Cumulative Use. J Clin Dent. 1998;9(4):83–8. PubMed: http://www.ncbi.nlm.nih.gov/pubmed/10518855

10 

Giani P. LAbbate ML, Kanapka J, Codipilly M, Kleinberg I. VSC inhibiting activity of experimental mouthwashes. J Dent Res. 1996;75:1422.

11 

Maeda M. Dermoscopic patterns of the filiform papillae of the tongue in patients with Sjögren’s syndrome. J Dermatol. 2006 Feb;33(2):96–102. DOI: http://dx.doi.org/10.1111/j.1346-8138.2006.00020.x PubMed: http://www.ncbi.nlm.nih.gov/pubmed/16556275

12 

de Beer D, Stoodley P, Roe F, Lewandowski Z. Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol Bioeng. 1994 May;43(11):1131–8. DOI: http://dx.doi.org/10.1002/bit.260431118 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/18615526

13 

Hess J, Greenman J, Duffield J. Modelling oral malodour from a tongue biofilm. J Breath Res. 2008 Mar;2(1):017003. DOI: http://dx.doi.org/10.1088/1752-7155/2/1/017003 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/21386147

14 

Kobayashi K, Kumakura M, Yoshimura K, Takahashi M, Zeng JH, Kageyama I, et al. Comparative morphological studies on the stereo structure of the lingual papillae of selected primates using scanning electron microscopy. Ann Anat. 2004 Dec;186(5-6):525–30. DOI: http://dx.doi.org/10.1016/S0940-9602(04)80101-8 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/15646287

15 

De Boever EH, Loesche WJ. Assessing the contribution of anaerobic microflora of the tongue to oral malodor. J Am Dent Assoc. 1995 Oct;126(10):1384–93. DOI: http://dx.doi.org/10.14219/jada.archive.1995.0049 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/7594010

16 

Quirynen M, De Soete M, Dierickx K, van Steenberghe D. The intra-oral translocation of periodontopathogens jeopardises the outcome of periodontal therapy. A review of the literature. J Clin Periodontol. 2001 Jun;28(6):499–507. DOI: http://dx.doi.org/10.1034/j.1600-051x.2001.028006499.x PubMed: http://www.ncbi.nlm.nih.gov/pubmed/11350516

17 

Mantilla Gómez S, Danser MM, Sipos PM, Rowshani B, van der Velden U, van der Weijden GA. Tongue coating and salivary bacterial counts in healthy/gingivitis subjects and periodontitis patients. J Clin Periodontol. 2001 Oct;28(10):970–8. DOI: http://dx.doi.org/10.1034/j.1600-051x.2001.028010970.x PubMed: http://www.ncbi.nlm.nih.gov/pubmed/11686816

18 

Winkel EG, Roldán S, Van Winkelhoff AJ, Herrera D, Sanz M. Clinical effects of a new mouthrinse containing chlorhexidine, cetylpyridinium chloride and zinc-lactate on oral halitosis. A dual-center, double-blind placebo-controlled study. J Clin Periodontol. 2003 Apr;30(4):300–6. DOI: http://dx.doi.org/10.1034/j.1600-051X.2003.00342.x PubMed: http://www.ncbi.nlm.nih.gov/pubmed/12694427

19 

Pérez JMM, Pascau J. Image Processing with ImageJ. 2013.

20 

Bernardi S, Zeka K, Mummolo S. Development of a new protocol: a macroscopic study of the tongue dorsal surface. Ital J Anat Embryol. 2013;118 2s:24.

21 

du Toit DF. The tongue: structure and function relevant to disease and oral health. SADJ. 2003 Oct;58(9):375–6, 380–3. PubMed: http://www.ncbi.nlm.nih.gov/pubmed/14964052

22 

Newman MG. The role of periodontitis in oral malodour: clinical perspectives. In: van Steenberghe, D; Rosenberg, M - editors. Bad Breath: A multidisciplinary approach. Leuven: Leuven University Press; 1996. p. 3-14.

23 

Kullaa-Mikkonen A, Järvinen J. Effects of age, sex and salivary secretion on the human tongue surface. Gerodontics. 1988 Jun;4(3):150–3. PubMed: http://www.ncbi.nlm.nih.gov/pubmed/3209037

24 

Kimori H, Yamamoto K, Yamachika S, Tsurumoto A, Kamikawa Y, Sasao M, et al. Factors associated with the presence of atrophic tongue in patients with dry mouth. Gerodontology. 2015 Mar;32(1):13–7. DOI: http://dx.doi.org/10.1111/ger.12045 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/23718267

25 

Murayama T, Kobayashi K. An Attempt at Replication of Human Lingual Papillae Using a Replica Method with Epoxy Resin. J Oral Biosci. 2007 Jan;49(2):143–9. DOI: http://dx.doi.org/10.1016/S1349-0079(07)80008-9

26 

Uemori N, Kakinoki Y, Karaki J, Kakigawa H. New method for determining surface roughness of tongue. Gerodontology. 2012 Jun;29(2):90–5. DOI: http://dx.doi.org/10.1111/j.1741-2358.2011.00509.x PubMed: http://www.ncbi.nlm.nih.gov/pubmed/21711389


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