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  Table of Contents  
ORIGINAL ARTICLE
Year : 2011  |  Volume : 48  |  Issue : 2  |  Page : 211-215
 

Stromal differences in odontogenic cysts of a common histopathogenesis but with different biological behavior: A study with picrosirius red and polarizing microscopy


Department of Oral Pathology and Microbiology, Subharti Dental College, Meerut, India

Date of Web Publication11-Jul-2011

Correspondence Address:
P Aggarwal
Department of Oral Pathology and Microbiology, Subharti Dental College, Meerut
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0019-509X.82897

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 » Abstract 

Objectives: The present study was undertaken to detect and compare the pattern of collagen fibers in odontogenic cysts and also to find out if this methodology could be used to predict the aggressive nature of odontogenic cysts by comparing with the odontogenic tumors. Materials and Methods: The collagen in the wall of 11 odontogenic keratocysts, 14 dentigerous cysts and 14 radicular cysts was studied histochemically by staining sections with picrosirius red and examining under polarizing microscope. This was compared to 10 cases of odontogenic tumors using Z test of proportion at 1% and 5%. Results: In dentigerous cysts, odontogenic keratocysts and odontogenic tumors, the predominant color of collagen fibers birefringence was found to be orangish red, whereas in radicular cysts the collagen fiber was of green color. Conclusions: Similar birefringence pattern of collagen fibers between dentigerous cysts, odontogenic keratocysts and odontogenic tumors may indicate that these lesions have a common histogenesis with a broad spectrum of biological behavior and belong to the same group, i.e., are developmental in origin. Different patterns of radicular cysts suggest different biological behavior and a positive role of inflammation on polarization color of collagen fibers.


Keywords: Collagen fibers, odontogenic cysts, picrosirius red, polarizing microscopy


How to cite this article:
Aggarwal P, Saxena S. Stromal differences in odontogenic cysts of a common histopathogenesis but with different biological behavior: A study with picrosirius red and polarizing microscopy. Indian J Cancer 2011;48:211-5

How to cite this URL:
Aggarwal P, Saxena S. Stromal differences in odontogenic cysts of a common histopathogenesis but with different biological behavior: A study with picrosirius red and polarizing microscopy. Indian J Cancer [serial online] 2011 [cited 2019 Aug 24];48:211-5. Available from: http://www.indianjcancer.com/text.asp?2011/48/2/211/82897



 » Introduction Top


Odontogenic cysts are usually classified into three main groups, namely, dental/radicular cysts, dentigerous cysts and odontogenic keratocysts. The proposed histogenetic differences and the clinically more aggressive behavior of odontogenic keratocysts compared with other cyst types has prompted studies aimed at characterizing possible differences between their fluid aspirates and epithelial linings. Little research has been done with respect to their connective tissue walls. [1]

Collagen plays a vital role in maintaining structural integrity and in determining tissue function. Therefore, methods to detect, quantify and analyze collagen are valuable. [2]

Picrosirius red stain, when used with polarized microscopy, not only characterizes collagenous material specifically and reliably, but also shows very clearly the orientation of collagen fibers. [2],[3]

The picrosirius-polarization methodology has occasionally been used in dental and gingival research to demonstrate pathological changes in collagen fibers, such as skin lesions, hyperplastic gingiva and odontogenic tumors. [4],[5],[6],[7] Very few studies have been done in odontogenic cysts using this stain.

This study was undertaken to detect and compare the pattern of collagen fibers in odontogenic cysts and also to find out if this methodology could be used to predict the aggressive nature of odontogenic cysts by comparing with the odontogenic tumors.


 » Materials and Methods Top


Thirty-nine cases of odontogenic cysts [11 odontogenic keratocysts (group 1), 14 dentigerous cysts (group 2), 14 radicular cysts (group 3)] and 10 cases of ameloblastoma (group 4) were retrieved from the files of the Oral Pathology and Microbiology Department. The diagnosis of the cysts and tumors was based on radiographic evidence, clinical description and histological features (H and E stained section).

Sections of 4 μm thickness were prepared, and after deparaffinization and hydration in distilled water, sections were incubated in 0.1% Sirius red F3B (C.I. 35780) in saturated picric acid solution for 1 hour at room temperature. This was followed by rinsing with distilled water, staining with Weigert's hematoxylin, differentiation in 1% acid alcohol, alkalinization with tap water, dehydration and mounting with Dibutylphathalate xylene (DPX).

To evaluate the birefringence pattern of collagen fibers, all the sections were examined under 4× magnification using Olympus polarized microscope. In odontogenic cysts, predominant colors of collagen fibers in connective tissue in relation to the epithelium were evaluated. For odontogenic tumors, the predominant color around islands was considered.

Data were read independently by three observers to eliminate inter-observer bias and were found to be comparable. The results were then tabulated and subjected to statistical analysis using Z test for proportion.


 » Results Top


In the present study, the predominant color of collagen fibers in stroma of odontogenic keratocysts, dentigerous cysts and odontogenic tumors was found to be orangish red [Figure 1], [Figure 2], [Figure 3], whereas in radicular cyst it was found to be green [Figure 4]. Whereas calculated Z value for all colours between Group 1 and group 4 [Table 1] and group 1 and group 2 [Table 2] was found to be nonsignificant.
Figure 1: Picrosirius red stained section of odontogenic keratocyst showing orangish red birefringence pattern of collagen fibers magnification (×4)

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Figure 2: Picrosirius red stained section of dentigerous cyst showing orangish red birefringence pattern of collagen fibers magnification (×4)

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Figure 3: Picrosirius red stained section of odontogenic tumor showing orangish red birefringence pattern of collagen fibers magnification (×4)

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Figure 4: Picrosirius red stained section of radicular cyst showing greenish yellow birefringence pattern of collagen fibers magnification (×4)

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Table 1: Comparison of birefringence pattern of collagen fibers between odontogenic keratocysts and odontogenic tumors (group 1 and group 4)

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Table 2: Comparison of birefringence pattern of collagen fibers between Odontogenic keratocyst (group 1) and dentigerous cysts (group 2)

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Using Z test for proportions, at 5% and 1% level of significance, the birefringence pattern of collagen fibers between different groups was compared. On comparing, the calculated Z values for greenish yellow color between group 2 and group 4 [Table 3], for green and orangish red between group 3 and group 4 [Table 4], for green and orangish red between group 1 and group 3 [Table 5], for green, greenish yellow and orangish red between group 2 and group 3 [Table 6] were found to be statically significant (P < 0.05).
Table 3: Comparison of birefringence pattern of collagen fibers between dentigerous cysts (group 2) and odontogenic tumors (group 4)

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Table 4: Comparison of birefringence pattern of collagen fibers between radicular cysts (group 3) and odontogenic tumors (group 4)

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Table 5: Comparison of birefringence pattern of collagen fibers between odontogenic cysts (group 1) and radicular cysts (group 3)

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Table 6: Comparison of birefringence pattern of collagen fibers between dentigerous cysts (group 2) and radicular cysts (group 3)

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 » Discussion Top


Epithelial-mesenchymal interactions are essential in maintaining homeostatic equilibrium in adult tissue, with the stromal cells maintaining control over cell size, function and response to wounds and other pathologic conditions through modification of the extracellular matrix (ECM). [8]

The ECM performs a very important role in growth regulation, tissue differentiation and organization. [9],[10]

Collagen is a major organic component that constitutes nearly 34% of the total ECM proteins. Type I and type III collagens are the most predominant types. [11],[12],[13]

It was observed that the collagens displayed different interference colors and intensities of birefringence, when studied by the picrosirius-polarization method, ranging from green to greenish yellow to yellow to orangish red, and red. [3],[14]

This can be explained by the widely known fact that these different interstitial collagens display distinct patterns of physical aggregation. [14] Collagen type I forms thick fibers composed of closely packed thick fibrils and consequently presents an intense birefringence with yellow to red color. Collagen type III (reticular fibers) forms thin fibers composed of loosely packed thin fibrils and thus displays a weak birefringence of a greenish color. [5],[7],[8],[9]

Recent studies have focused on the importance of the epithelial-mesenchymal interactions in odontogenic cysts and have demonstrated that the expansion involves degradation of bone matrix and cell attachment to the ECM components. [15],[16],[17]

Vedtofte et al, demonstrated that transplanted keratocyst epithelium in nude mice retained its typical histological appearance only when supported by its own stroma. Thus, it can be suggested that the biological behavior of odontogenic keratocyst is dependent not only on the epithelium but also on the underlying stroma. [18]

The capsule essentially is composed of collagen fibers consisting of both thin and thick fibers arranged in bundles. The nature of arrangement in odontogenic cysts is little understood.

Hirsberg et al, used picrosirius red to note the differences in collagen in odontogenic cysts. [19]

In the present study, the predominant color of collagen fibers in stroma of odontogenic keratocysts and dentigerous cysts was found to be orangish red. When comparison between these two groups was done, there was no significant difference statistically (P > 0.05). The predominant color in radicular cysts in 10 out of 14 cases (71.43%) was green and the other 4 cases showed greenish yellow birefringence.

In our study, green to greenish yellow color of collagen fibers in radicular cysts suggests that the collagen found in these lesions is loosely packed and might be composed of procollagens, intermediate or pathologic collagens rather than the normal tightly packed fibers seen in dentigerous cysts and odontogenic keratocysts. This could be explained by the fact that the radicular cyst is an inflammatory cyst and the inflammatory cells could affect the packing of collagen fibers. [8]

Teronan et al, held the view that macrophages and neutrophils have a common feature of elaboration of a tissue collagenase, which is capable of causing hydrolytic breakdown of peptide bonds in the helical region of collagen. Collagenolytic activity is least in normal and mildly inflamed tissue and greatest in severely inflamed hyperplastic tissue. Thus, inflammatory cells could affect the arrangement of collagen. [15],[16],[17]

In the present study, the predominant color of collagen fibers around the tumor islands in odontogenic tumors was orangish red. When the comparison of color of collagen fibers of odontogenic tumors with that of odontogenic keratocysts and dentigerous cysts was done, there was no significant difference statistically (P > 0.05). When odontogenic tumors were compared to radicular cysts, there was a statistically significant difference between these two groups (P < 0.05).

The present study shows that connective tissue stroma of odontogenic keratocysts, dentigerous cysts and odontogenic tumors predominantly exhibited orangish red collagen fibers, which may suggest that they belong to the same group, i.e., are developmental in origin, and their longstanding nature might be the cause of closely packed collagen fibers.

Zegarelle concluded from his investigations of induced ameloblastoma in mice that odontogenic cysts are stages in the development of ameloblastoma. [20]

Spouge postulated a "Unitarian concept" that relates the histology and clinical behavior of odontogenic tumors to the embryonic properties and functions and to the degree of differentiation of their appropriate parent tissue. This theory brings ameloblastoma and odontogenic cysts under the same category, which may help to clarify their relationship. [21]

It can be concluded from our study that similarity between dentigerous cysts, odontogenic keratocysts and odontogenic tumors may indicate that these lesions have a common histogenesis with a broad spectrum of biological behavior.


 » Conclusions Top


Similar collagen characterization of dentigerous cysts, odontogenic keratocysts and odontogenic tumors provides further evidence regarding the comparable nature and biological behavior of these lesions. Hence, the treatment modality of these developmental cysts may be compared to that of odontogenic tumors.

On the other hand, the dissimilar pattern of collagen arrangement in radicular cysts suggests a different biological behavior, thus warranting a more conservative treatment and a positive role of inflammation on the polarization color characteristic of collagen fibers.

From the present study, we can suggest that the connective tissue stroma of odontogenic cysts may be regarded as a functional part of the cyst and not just a structural support.

 
 » References Top

1.Browne RM. The pathogenesis of odontogenic cysts: A review. J Oral Pathol 1975;4:31-46.  Back to cited text no. 1
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2.Whittaker P, Rich L. Collagen and picrosirius red staining: A polarized light assessment of fibrillar hue and spatial distribution. Braz J Morphol Sci 2005;22:97-104.  Back to cited text no. 2
    
3.Junqueria LC, Bignolos G, Brentani RR. Picrosirius staining plus polarizing microscopy: A specific method for collagen detection in tissue sections. Histochem J 1979;11:447-55.  Back to cited text no. 3
    
4.Trau H, Dayan D, Hirshberg A, Hiss Y, Bubis JJ. Wolman M. Connective tissue nevi collagens: Study with picrosirius red and polarizing microscope. Am J Drematopathol 1991;13:374-7.  Back to cited text no. 4
    
5.Dayan D, Waner T, Tal H, Nyska A. Polarization microscopy of picrosirius red-stained collagen from oxidipine-induced hyperplastic gingival of beagle dogs. Int J Exp Pathol 1993;74:225-8.  Back to cited text no. 5
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6.Nysha A, Dayan D. Ameloblastic fibroma in a young cat. J Oral Pathol Med 1995;24:233-6.  Back to cited text no. 6
    
7.Hirshberg A, Buchner A, Dayan D. The central odontogenic fibroma and the hyperplastic dental follicle: Study with picrosiruis red and polarizing microscopy. J Oral Pathol Med 1996;25:125-7.  Back to cited text no. 7
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8.Hirshberg A, Lib M, Kozlovsky A, Kaplan I. The influence of inflammation on polarization color of collagen fibers in the wall of odontogenic Keratocyst. Oral Oncol 2007;43:278-82.  Back to cited text no. 8
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9.Allon I, Vered M, Buchner A , Dayan D. Stromal differences in salivary gland tumors of a common histopathogenesis but with different biological behavior: A study with picrosirius red and polarizing microscopy. Acta Histochem 2006;108:259-64.   Back to cited text no. 9
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10.Becker J, Riechart S, Philipsen HP. Ectomesenchyme of ameloblastic fibroma reveals a characteristic distribution of extracellular matrix proteins. J Oral Pathol med 1992;21:156-9.  Back to cited text no. 10
    
11.Nimmi ME. Collagen: Its structure and function in normal and pathological connective tissues. Semin Arthritis Rheumat 1974;4:95-150.  Back to cited text no. 11
    
12.Junqueira LC, Montes GS, Martins JE, Joazeiro PP. dermal collagen distribution: A histochemical and ultrastructural study. Histochemistry 1983;79:397-403.  Back to cited text no. 12
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13.Narayanan SA, Page RC. Biochemical characterization of collagens synthesized by fibroblasts derived from normal and diseased human gingiva. J Biol Chem 1976;25:5464-71.  Back to cited text no. 13
    
14.Junqueria LC, Montes GS, Sanchez EM. The influence of tissue section thickness on the study of collagen by the picrosirius-polarization method. Histochemistry 1982;74:153-6.  Back to cited text no. 14
    
15.Teronen O, Salo T, Laitinen J, Törnwall J, Ylipaavalneiemi P, Konttinen YT, et al. Characterization of interstitial collagenases in jaw cyst wall. Eur J Oral Sci 1995;103:141-7.  Back to cited text no. 15
    
16.Teonen O, Salo T, Konttinen YT, Rifkin B, Vernillo A, Ramamurthy NS, et al. Identification and characterization of gelatinases /type IV collagenases in jaw cysts. J Oral Pathol Med 1995;24:78-84.  Back to cited text no. 16
    
17.Megha JS, Harvey M. Interleukin 1- like activity in cystic lesions of the jaw. Br J Oral Maxillofacial Surg 1989;27:1-11.  Back to cited text no. 17
    
18.Vedtofte P, Holmstrup P, Dabelsteen E. Human odontogenic keratocyst transplant in nude mice. Scand J Dent Res 1982;90:306- 14.  Back to cited text no. 18
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19.Hirshberg A, Sherman S, Buchner A, Dayan D. Collagen fibres in the wall of odontogenic keratocysts: A study with picrosirius red and polarizing microscopy. J Oral Pathol Med 1999;28:410-2.  Back to cited text no. 19
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20.Zegarelli EV. Admantinoblastoma in the style stock of mice. Am J Pathol 1994;20:23-6.  Back to cited text no. 20
    
21.Spongue JD. Odontogenic tumors: A Unitarian concept. Oral Surg 1967;24:392-5.  Back to cited text no. 21
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]

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