Development of Candida-associated denture stomatitis: new insights

REVIEW

Development of Candida-associated denture stomatitis: new insights

Tatiana Pereira-Cenci^I; Altair Antoninha Del Bel Cury^II; Wim Crielaard^III; Jacob Martien Ten Cate^III

^IDDS, MSc, Graduate student, Department of Prosthodontics and Periodontology, Dental School of Piracicaba, State University of Campinas, SP, Brazil

^IIDDS, Msc, PhD, Associate Professor, Department of Prosthodontics and Periodontology, Dental School of Piracicaba, State University of Campinas, SP, Brazil

^IIIBSc, Msc, PhD, Full Professor, Department of Cariology, Endodontology Pedodontology, Academic Centre for Dentistry Amsterdam, ACTA, Amsterdam, Netherlands

^{Corresponding address}

ABSTRACT

Despite therapeutic progress, opportunistic oral fungal infectious diseases have increased in prevalence, especially in denture wearers. The combination of entrapment of yeast cells in irregularities in denture-base and denture-relining materials, poor oral hygiene and several systemic factors is the most probable cause for the onset of this infectious disease. Hence colonization and growth on prostheses by Candida species are of clinical importance. The purpose of this review is to critically discuss several key factors controlling the adhesion of Candida species which are relevant to denture-associated stomatitis. Although there is some consensus on the role of surface properties, studies on several other factors, as the use of denture liners, salivary properties and yeast-bacterial interactions, have shown contradictory findings. A comprehensive fundamental understanding is hampered by conflicting findings due to the large variations in experimental protocols, while other factors have never been thoroughly studied. Surface free energy and surface roughness control the initial adherence, but temporal changes have not been reported. Neither have in vivo studies shown if the substratum type is critical in dictating biofilm accumulation during longer periods in the oral environment. The contribution of saliva is unclear due to factors like variations in its collection and handling. Initial findings have disclosed that also bacteria are crucial for the successful establishment of Candida in biofilms, but the clinical significance of this observation is yet to be confirmed. In conclusion, there is a need to standardize experimental procedures, to bridge the gap between laboratory and in vivo methodologies and findings and - in general - to thoroughly investigate the factors that modulate the initial attachment and subsequent colonization of denture-base materials and the oral mucosa of patients subjected to Candida infections. Information on how these factors can be controlled is required and this may help to prevent the disease. The societal impact of such information is significant given the magnitude of the candidosis problem worldwide.

Key words:Candida albicans. Biofilm. Denture. Saliva. Bacteria.

INTRODUCTION

Candida infections receive increasing attention, presumably due to the increased prevalence worldwide. Numerous studies have shown that several Candida species possess a multitude of virulence mechanisms leading to successful colonization and infection of the host when suitable conditions occur. The recognition that Candida is an important pathogen has led to many laboratory studies evaluating these virulence attributes in an attempt to clarify the pathogenesis of the disease. The progress made in understanding some of these features, such as the mechanisms that result in adherence to surfaces⁷⁹, cell surface hydrophobicity³², and saliva¹³ is very impressive though yet in many aspects inconclusive. Knowledge about how the adherence and biofilm formation process takes place and how to avoid or at least diminish Candida colonization are mandatory in clinical practice. This review aims to critically discuss several key factors controlling the adhesion of Candida species which are relevant to denture-associated stomatitis, to highlight areas of current controversy and to suggest future research.

Role of surface properties on Candida colonization

Fungi normally live as innocuous commensals and colonize various habitats in humans, notably skin and mucosa^63,88. Commensal existence of oral Candida species varies from 20% to 50% in a healthy dentulous population^79,88. As growth on surfaces is a natural part of the Candida lifestyle⁵¹, one can expect that Candida colonizes denture.

There is a large body of evidence indicating that Candida is able to adhere to acrylic resin dentures. This is the first step that may lead to the development of the infectious process and that may ultimately result in varying degrees of denture stomatitis of the adjacent mucosa^13,15,84. Candida adheres directly or via a layer of denture plaque to denture base (polymethylmethacrylate - PMMA)^7,23,86. Without this adherence, micro-organisms would be removed from the oral cavity when saliva or food is being swallowed.

It is well-known that innumerable factors are involved in the adhesion of Candida to the acrylic resin base, though contradictory results have been reported from in vitro studies^68,78,93. Substrate surface properties, as surface charge, surface free energy, hydrophobicity, and roughness have all been reported to influence the initial adhesion of micro-organisms^8,104. Microbial adhesion on biomaterial surfaces depends on the surface structure and composition of biomaterials, and on the physicochemical properties of the microbial cell surface, again its surface charge and hydrophobicity^4,11. Components of the resilient denture liners and acrylic resin may reduce the adhesion and inhibit the growth of Candida^45,105,108.

(a) Surface free energy and surface roughness

Surface free energy is one of the main factors related to the development of denture related candidosis⁶⁷. It is defined as the interaction between the forces of cohesion and adhesion and predicts whether or not wetting occurs¹¹³. A linear relationship between contact angle measurements on various types of substratum and Candida albicans adherence has been demonstrated, i.e. the higher the surface free energy, the higher will be the adhesion of micro-organisms and alternatively, the more hydrophobic the surface, the less cell adherence is expected^33,45,67.

Although the cited reports have found correlations between surface free energy and microbial' adhesion¹², other factors should also be considered, such as cell surface factors, diet, salivary composition and secretion rates, and antibody titers, which are all controlling factors in plaque formation⁹ and could therefore influence yeast attachment. These many confounding factors might explain why recent studies have failed to show a direct correlation between surface free energy values and the adhesion of Candida species^68,78,93,110.

Higher adherence of particular Candida species, e.g. C. tropicalis, C. glabrata and C.dubliniensis, when compared with C. albicans, might be attributed to their relative surface free energy values, since hydrophobic micro-organisms seem to be more adherent to acrylic surfaces. While there are no studies regarding hydrophobicity of C. tropicalis and C. dubliniensis, Luo and Samaranayake⁵⁵ (2002) stated that C. glabrata is more hydrophobic than C. albicans.

Commonly used biomaterials exhibit significant differences in surface free energy. Heat-polymerized acrylic resin was reported to be more wettable than microwave-polymerized acrylic resin, due to acid-base interactions^68,94.

Surface roughness is calculated as the arithmetic average deviation of the surface valleys and peaks of a given surface¹. It directly influences micro-organisms initial adherence to surfaces, biofilm development, and Candida species colonization. Materials with the roughest surface usually exhibit higher yeast counts^70,78,83,105. This happens because surfaces may serve as a reservoir, with surface irregularities providing an increased chance of micro-organism retention and protection from shear forces, even during denture cleaning. In addition, these irregularities sometimes allow the entrapped microbial cells time to attach irreversibly to a surface⁹⁸.

Quirynen, et al.⁷⁹ (1990) postulated a threshold roughness value (0.2 mm) below which no effect on the adhesion should be expected. Smooth and highly polished surfaces are of utmost importance not only for patient's comfort but also for denture/restoration longevity, good aesthetical results, oral hygiene and low plaque retention¹⁰¹.

The presence of saliva is known to change this scenario. The nature of the substratum may influence the formation and the composition of the salivary pellicle, which layer may then become more relevant than the surface properties of the dental material itself³⁰. It has been shown that saliva immersion decreases the surface roughness⁸³ and surface free energy⁹⁴ of acrylic resins. This might explain the general decrease of Candida species in those studies where specimens were coated with saliva. Saliva, its components and properties on Candida adherence and colonization is thoroughly discussed in the following paragraph Role of the salivary properties on Candida colonization.

The available studies on surface properties raise questions regarding the role of surface free energy and surface roughness. There is general agreement that the hydrophobicity of the cell surface and substratum is an important predictor in the adhesion process, i.e. surface free energy indicates the ease with which saliva spreads over a surface^67,94. There is also consensus on the role of surface roughness and the initial adherence process, i.e. surface roughness is positively correlated with the rate of bacterial/fungal colonization of biomaterials. If such rougher surfaces become exposed to the oral environment, they may be more susceptible to micro-organisms adhesion and biofilm formation and lead to infections. However, no studies on the application of certain treatments on different substratum types have been reported (i.e. application of different treatments diminishes the number of yeasts but may lead to detrimental changes of the substratum). In vivo studies may lead to different outcomes when compared with in vitro studies.

(b) Denture liners surface and characteristics

New materials have been developed in order to reduce and redistribute occlusal forces from dentures that might damage the underlying mucosal tissues^60,97. In recent years, the use of denture liners, either hard or soft, has increased.

Liners are needed in many clinical situations in which patients have thin, sharp, or badly resorbed residual alveolar ridges or chronic tissue irritation from dentures^57,60. Even though these materials exhibit excellent tissue tolerance, one of the problems is the colonization of Candida spp. on and within the material. Fungal growth is known to destroy the surface properties of the liner and this may lead to irritation of the oral tissues. This is due to a combination of increased surface roughness and high concentrations of exotoxins and metabolic products produced by the fungal colonies⁵⁷. This observation is the rationale why attempts have been undertaken to incorporate antifungal agents or antiseptics in these materials.

Unfortunately, conflicting adherence/colonization results are reported on these lining materials. Some in vitro studies reported significant inhibitory effects on C. albicans^21,112. More recent studies, however, showed only limited antifungal properties and no significant reduction on Candida adherence and colonization^{17,21,24,31,49,50,53,58,75,78} .

As can be seen in Figure 1A and ^B and as was also reported previously¹⁰⁵, denture liners, especially the soft ones, introduce a higher surface roughness. The porous surface texture of the material will entrap yeast cells (Figure 2A and ^B), leading to an increased (re)colonization in spite of the antifungals. Concomitantly, the nutrient-rich environment of the oral cavity might overrule any inhibitory effect induced by antifungals released from the denture liners³¹.

Even though some in vitro studies have shown limited inhibitory effects, a reasonable explanation on why lining materials do not keep their antifungal characteristics could be the constant bathing in saliva in the mouth. Saliva extracts the antifungal ingredients, possibly even within a short time after the denture is placed in the oral environment, or dilutes the concentration near the denture surface to below fungicidal concentrations. Moreover, the antifungal included might not be effective against the particular Candida species (or mixture of micro-organisms, see below) that is causing the infection. Judging the literature the need emerges to systematically evaluate liners against various Candida species in relevant assays, e.g. involving various Candida and bacterial mixtures and saliva.

Role of salivary properties on Candida colonization

The role of human saliva in the Candida adhesion process is still controversial^68,73. Saliva shows a physical cleaning effect and innate defence molecules, including lysozyme, histatin, lactoferrin, calprotectin and IgA^20,96, interact with Candida species, thereby decreasing adherence to and colonization of oral surfaces. Other components in whole saliva, including mucins^20,25, statherin⁴² and proline-rich-proteins^13,96 have been reported to adsorb to C. albicans, thereby facilitating adherence to saliva-coated acrylic resins².

However, studies regarding the influence of whole saliva on Candida adherence are mutuality contradictory and no consensus can be found in the literature (Table 1). Several investigators reported that a saliva coating reduces the adherence of C. albicans in acrylic resin based materials^{6,59,65,66,68,72,78,86,110} Others showed increased adherence rates with saliva coating^23,65,71,102. Three other research groups found no effect at all of a saliva coating^41,72,97. A dynamic effect, depending on the morphological phase of C. albicans was also found^84,91, where initially adherence was increased, but subsequently decreased after 24 hours.

Several reasons might explain these divergent results. The most important are probably differences in the use of stimulated versus unstimulated saliva, resulting in different protein composition and viscosity, hence protection¹⁰³. Furthermore, different incubation periods, use of filtered or whole saliva, different saliva temperatures when performing the study, and the presence or absence of nutrients in the different studies may have interfered with cell viability and adherence capacity^20,41,83,86. Obviously inter-individual variations in the composition of saliva affect the outcome of three component adherence system studies of substratum, saliva and yeast^{19,25,68,73,78}.

In the oral cavity a denture is coated with a salivary pellicle, which provides receptor sites for the adherence of micro-organism²⁸. Again surface roughness and surface free energy are confounding factors in the coating. Although surface characteristics are important in determining the final composition of an acquired pellicle and hence can dictate colonization of Candida species, there are only few studies where the effects of different types of acrylic resins on this process are compared^67,83.

Studies dealing with the effect of saliva on adherence of Candida species, other than C. albicans, to acrylic resins in vitro and in vivo, indicate variable adherence levels^66,68,78. C. dubliniensis counts have been shown to decrease²⁵, increase⁸⁵ or show no effect⁶⁸ in the presence of saliva, while C. glabrata counts were not influenced by saliva in one study⁶⁸ but decreased in another report⁷⁸.

Thus there is contradicting evidence with regard to the relationship in vitro between saliva and Candida adhesion. In general it may be concluded that low molecular weight proteins are related to the adherence levels of Candida¹⁰. This is in agreement with clinical studies^20,74,80,96, where patients with low or impaired salivary flow and/or composition presented higher Candida species counts when compared with saliva from patients with normal salivary flow. Collectively this confirms the regulating role of saliva in inhibiting Candida species adherence.

Candida species' shift

The Candida species most often reported to be associated with oral mucosal lesions is Candida albicans. But C. tropicalis, C. parapsilosis, C. glabrata, C. krusei, and C. dubliniensis have also been isolated from diseased tissues^18,56,89,90. Recently a shift in disease-associated Candida species from Candida albicans towards these non-albicans species was observed^48,87,107. While C. albicans is still by far the predominant isolate under inflammatory conditions³⁴, C. glabrata emerges as the second most prevalent species, frequently isolated from acrylic denture surfaces and the palatal mucosa⁸⁹. Candida glabrata used to be considered a non-pathogenic Candida species, but the increased use of immunosuppressive drugs, as a cure of the immunosuppressive syndrome, have now led to increasing C. glabrata infections with high mortality rates⁴⁷. The explanation for this trend towards morbidity due to ''less pathogenic'' yeasts remains to be established, but it has already been suggested that the increased worldwide use of antifungals has contributed to this phenomenon^92,95. Besides the shift from C. albicans to C. glabrata, there is increasing evidence that more than one Candida species may simultaneously colonize mucosal habitats, as reported for the oral mucosa²², tongue and palate⁹², both in healthy and diseased subjects.

Bacteria and Candida interactions

Microbial cell to cell communication plays an important role in the colonization process. Micro-organisms present in the oral environment interact with each other in many ways, such as by using each other's metabolic end-products, or by communicating more directly through signalling molecules⁵. Understanding the complex interactions between surfaces, saliva, eukaryotic and prokaryotic micro-organisms during infections is crucial in developing prevention and treatment strategies. In studies on Candida biofilm formation and Candida susceptibility, the characteristics of the oral environment in which the biofilms are naturally formed should be mimicked as closely as feasible⁵².

The multicellular lifestyle of bacterial and yeast biofilms^44,69 is induced by environmental stress and/or restricted nutrient supplies⁷⁶. These cooperation lead to adaptation to natural stress responses and result in a balanced microflora^62,64,76,77. In addition to various forms of metabolic dependence micro-organisms may co-aggregate, with two or more genetically distinct strains interacting through specific cell to cell recognition³⁸. Such co-aggregation has been observed between C. albicans and several other oral micro-organisms^36,37,39 and is an important factor in the microbial colonization and progression of infections in the oral cavity.

Bacteria and yeasts also interact via quorum sensing (QS). Quorum sensing is a polymicrobial coordination within a microbial community, based on excreted small molecules triggering a genetic response when present in sufficiently high concentrations. QS occurs both in single species bacterial communities and in complex mixed bacterial-yeast communities^16,43. A recent study³⁵ showed that Candida hyphal formation can be modulated by Gram negative bacterial quorum sensing molecules. Particularly in the multispecies biofilm communities QS molecules may accumulate to high concentrations and hence are important in controlling physiology and homeostasis⁴⁶.

Although studies on biofilm development and species interactions have, so far, focused largely on bacterial species it has become clear that synergistic interactions among micro-organisms increase the efficiency of the impropagation^29,54. Oral biofilm are not random mixtures of micro-organisms; but organized structures though varying in space and time while modulating adherence and metabolic properties⁹⁹. Immediately after brushing or prophylaxis, the surface will be recoated with salivary pellicle and the first pioneer bacteria will colonize. These "early colonizers" are followed by the "late colonizers", if the conditions of/in the biofilm become amenable for other species to survive⁴⁰.

Although there is variability in composition of an oral biofilm community depending on patient dependent characteristics, the mere presence of a specific micro-organism does not induce pathology. Typically this depends on a complex of micro-organisms-host interactions that modulate the host's response leading to inflammation. Depending on the local conditions, bacteria may provide fungi with compounds that activate virulence determinants of fungi¹⁰⁹. This is not only important for Candida infections but also why Candida may be responsible for non-Candida infections induced by the patient's indigenous microflora²⁷.

Several researchers have studied interactions among Candida and bacteria in an attempt to determine how oral bacteria may modulate Candida adherence and colonization. The influence of Streptococcus salivarius has been reported to decrease Candida adherence⁸⁶, while cooperation between several Streptococci and Candida albicans has also been reported^7,106. Other research groups assessed in vivo biofilms, with various plaque collection methods generally destructive to the biofilm structure^{14,26,82,84,111}. In contrast, the new confocal scanning laser microscopy using molecular biological staining techniques may elucidate unsolved issues or even identify artefacts arising from traditional methodologies. A recent study using acrylic resin samples of denture wearers in vivo has shown that different subjects present different biofilm formation rates, architecture and densities³. Unfortunately, the only substratum tested was acrylic resin and there was no attempt to characterize the surface properties, which might have resulted in a better understanding of the process. Clearly, understanding the biofilm behaviour of Candida species under various environmental conditions is the key to the development of effective preventive measures for Candida infections¹⁰⁰. Further studies are needed to establish whether or not these interactions are strain-specific and on which other parameters they depend. As a result it may be possible to identify the stages when C. albicans and other emerging pathogenic species can be targeted in treatment and prevention.

Future research and final remarks

From the literature the picture emerges that many factors determine Candida harbouring biofilms. These factors include surface properties, micro-organisms interactions, biofilm architecture, and saliva. Obviously it is tempting to study the individual parameters in simple mechanistic studies. However, the level of contradictions in the pertaining literature should be interpreted by assuming multiple interactions between the various factors. A meaningful study of Candida biofilms thus only seems possible when the various factors are studied in a comprehensive experimental design.

As recent studies are pointing to the role of multi-species biofilms on the onset of the disease, studies that may explain how such biofilms interact with surfaces and how to prevent their growth are important. Fungal adhesion may be greater in materials presenting higher surface roughness. Consequently, the rehabilitation material chosen in clinical situations has to be carefully considered. When the oral cavity is re-colonized after antimycotic treatment withdrawal in patients with oral candidiasis, the yeasts may be harboured in more remote sites of the material.

While the initial adhesion of Candida species is influenced by surface roughness, and may be influenced by the materials' surface free energy (question still under discussion), these characteristics should be evaluated in in vivo-like conditions. Indeed, the presence of a rehabilitation material that could favour health and avoid the oral cavity re-colonization is mandatory. Therefore, studies that could explore the factors related to initial re-colonization by Candida in different materials are of utmost importance. The relationship of denture base materials and their effect on fungal growth requires further investigation through epidemiologic, clinical, and basic research. These new studies may include surface characteristics, but other important matters discussed on this review are fundamental to facilitate treatment protocols. New research should be on multispecies biofilm, as close as possible to the in vivo situation. Furthermore, other emerging fungal pathogens, such as Candida glabrata, should be under investigation, as the results found for one Candida species (mainly Candida albicans) may not generally hold, again in experimental setups where other organisms and saliva are present.

Received: November 22, 2007

Modification: January 10, 2008

Accepted: February 6, 2008

• 1- Anusavice KJ. Philips' science of dental materials. 10th ed. Pennsylvania: W.B. Saunders, 1996. p.273-300.
• 2- Arendorf TM, Walker DM. Denture stomatitis: a review. J Oral Rehabil. 1987;14:217-27.
• 3- Avon SL, Goulet JP, Deslauriers N. Removable acrylic resin disk as a sampling system for the study of denture biofilms in vivo J Prosthet Dent. 2007;97:32-8.
• 4- Bellon-Fontaine MN, Mozes N, van der Mei HC, Sjollema J, Cerf O, Rouxhet PG, Busscher HJ. A comparison of thermodynamic approaches to predict the adhesion of dairy microorganisms to solid substrata. Cell Biophys. 1990;17:93-106.
• 5- Blankenship JR, Mitchell AP. How to build a biofilm: a fungal perspective. Curr Opin Microbiol. 2006;9:588-94.
• 6- Bosch JA, Turkenburg M, Nazmi K, Veerman EC, de Geus EJ, Nieuw Amerongen AV. Stress as a determinant of saliva-mediated adherence and coadherence of oral and nonoral microorganisms. Psychosom Med. 2003;65:604-12.
• 7- Branting C, Sund ML, Linder LE. The influence of Streptococcus mutans on adhesion of Candida albicans to acrylic surfaces in vitro Arch Oral Biol. 1989;34:347-53.
• 8- Bridgett MJ, Davies MC, Denyer SP, Eldridge PR. In vitro assessment of bacterial adhesion to Hydromer-coated cerebrospinal fluid shunts. Biomaterials. 1993;14:184-8.
• 9- Budtz-Jorgensen E, Theilade E, Theilade J. Quantitative relationship between yeast and bacteria in denture-induced stomatitis. Scand J Dent Res. 1983; 91:134-42.
• 10- Busscher HI, Geertsema-Doornbusch GI, van der Mei HC. Adhesion to silicone rubber of yeasts and bacteria isolated from voice prostheses: influence of salivary conditioning films. J Biomed Mater Res. 1997;34:201-10.
• 11- Busscher HJ, Cowan MM, van der Mei HC. On the relative importance of specific and non-specific approaches to oral microbial adhesion. FEMS Microbiol Rev. 1992;8:199-209.
• 12- Busscher HJ, Weerkamp AH, van der Mei HC, van Pelt AW, de Jong HP, Arends J. Measurement of the surface free energy of bacterial cell surfaces and its relevance for adhesion. Appl Environ Microbiol. 1984;48:980-3.
• 13- Cannon RD, Chaffin WL. Oral colonization by Candida albicans Crit Rev Oral Biol Med. 1999;10:359-83.
• 14- Catalan A, Herrera R, Martinez A. Denture plaque and palatal mucosa in denture stomatitis: scanning electron microscopic and microbiologic study. J Prosthet Dent. 1987;57:581-6.
• 15- Chandra J, Mukherjee PK, Leidich SD, Faddoul FF, Hoyer LL, Douglas LJ, Ghannoum MA. Antifungal resistance of candidal biofilms formed on denture acrylic in vitro J Dent Res. 2001;80:903-8.
• 16- Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL, Hughson FM. Structural identification of a bacterial quorum-sensing signal containing boron. Nature. 2002;415:545-9.
• 17- Chow CK, Matear DW, Lawrence HP. Efficacy of antifungal agents in tissue conditioners in treating candidiasis. Gerodontology. 1999;16:110-8.
• 18- Coleman DC, Sullivan DJ, Bennett DE, Moran GP, Barry HJ, Shanley DB. Candidiasis: the emergence of a novel species, Candida dubliniensis AIDS. 1997;11:557-67.
• 19- Dar-Odeh NS, Shehabi AA. Oral candidosis in patients with removable dentures. Mycoses. 2003;46:187-91.
• 20- Dodds MW, Johnson DA, Yeh CK. Health benefits of saliva: a review. J Dent. 2005;33:223-33.
• 21- Douglas WH, Walker DM. Nystatin in denture liners- an alternative treatment of denture stomatitis. Br Dent J. 1973;135:55-9.
• 22- Dronda F, Alonso-Sanz M, Laguna F, Chaves F, 93 - Martinez-Suarez JV, Rodriguez-Tudela JL, Gonzalez-Lopez A, Valencia E. Mixed oropharyngeal candidiasis due to Candida albicans and non-albicans Candida strains in HIV-infected patients. Eur J Clin Microbiol Infect Dis. 1996;15:446-52.
• 23- Edgerton M, Scannapieco FA, Reddy MS, Levine MJ. Human submandibular-sublingual saliva promotes adhesion of Candida albicans to polymethylmethacrylate. Infect Immun. 1993;61:2644-52.
• 24- el-Charkawi H, el-Said EA, Safouh HM, el-Raghi N. Effect of addition antimicrobial agents to denture reliners. Egypt Dent J. 1994;40:785-90.
• 25- Elguezabal N, Maza JL, Ponton J. Inhibition of adherence of Candida albicans and Candida dubliniensis to a resin composite restorative dental material by salivary secretory IgA and monoclonal antibodies. Oral Dis. 2004;10:81-6.
• 26- Frank RM, Steuer P. Transmission electron microscopy of plaque accumulations in denture stomatitis. J Prosthet Dent. 1985;53:115-24.
• 27- Fridkin SK, Jarvis WR. Epidemiology of nosocomial fungal infections. Clin Microbiol Rev. 1996,9:499-511.
• 28- Garcia RM, Léon BT, Oliveira VB, Del Bel Cury AA. Effect of a denture cleanser on weight, surface roughness, and tensile bond strength of two resilient denture liners. J Prosthet Dent. 2003;89:489-94.
• 29- Garcia de Viedma D, Lorenzo G, Cardona PJ, Rodriguez NA, Gordillo S, Serrano MJ, Bouza E. Association between the infectivity of Mycobacterium tuberculosis strains and their efficiency for extrarespiratory infection. J Infect Dis. 2005;192:2059-65.
• 30- Gocke R, Gerath F, von Schwanewede H. Quantitative determination of salivary components in the pellicle on PMMA denture base material. Clin Oral Investig. 2002;6:227-35.
• 31- Graham BS, Jones DW, Burke J, Thompson JP. In vivo fungal presence and growth on two resilient denture liners. J Prosthet Dent. 1991;65:528-32.
• 32- Hazen KC, Brawner DL, Riesselman MH, Jutila MA, Cutler JE. Differential adherence of hydrophobic and hydrophilic Candida albicans yeast cells to mouse tissues. Infect Immun. 1991;59:907-12.
• 33- Hazen KC. Participation of yeast cell surface hydrophobicity in adherence of Candida albicans to human epithelial cells. Infect Immun. 1989;57:1894-1900.
• 34- He XY, Meurman JH, Kari K, Rautemaa R, Samaranayake LP. In vitro adhesion of Candida species to denture base materials. Mycoses. 2006;49:80-4.
• 35- Hogan DA, Vik A, Kolter R. A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol. 2004;54:1212-23.
• 36- Holmes AR, Gopal PK, Jenkinson HF. Adherence of Candida albicans to a cell surface polysaccharide receptor on Streptococcus gordonii Infect Immun. 1995;63:1827-34.
• 37- Hsu LY, Minah G, Peterson DE, Wingard JR, Merz WG, Altomonte V, Tylenda CA. Coaggregation of oral Candida isolates with bacteria from bone marrow transplant recipients. J Clin Microbiol. 1990;28:2621-6.
• 38- James A, Beaudette L, Costerton W. Interspecies bacterial interactions in biofilms. J Industrial Microbiol. 1995;15:257-62.
• 39- Jenkinson HF, Lala HC, Shepherd MG. Coaggregation of Streptococcus sanguis and other streptococci with Candida albicans Infect Immun. 1990;58:1429-36.
• 40- Jenkinson HF, Lamont RJ. Oral microbial communities in sickness and in health. Trends Microbiol. 2005;13:589-95.
• 41- Jin Y, Samaranayake LP, Samaranayake Y, Yip HK. Biofilm formation of Candida albicans is variably affected by saliva and dietary sugars. Arch Oral Biol. 2004;49:789-98.
• 42- Johansson I, Bratt P, Hay DI, Schluckebier S, Stromberg N. Adhesion of Candida albicans, but not Candida krusei, to salivary statherin and mimicking host molecules. Oral Microbiol Immunol. 2000;15:112-8.
• 43- Keller L, Surette MG: Communication in bacteria: an ecological and evolutionary perspective. Nat Rev Microbiol. 2006;4:249-58.
• 44- Kierek-Pearson K, Karatan E. Biofilm development in bacteria. Adv Appl Microbiol. 2005;57:79-111.
• 45- Klotz SA, Drutz DJ, Zajic JE. Factors governing adherence of Candida species to plastic surfaces. Infect Immun. 1985;50:97-101.
• 46- Koo H, Schobel BD, Scott-Anne K, Watson G, Bowen WH, Cury JA, Rosalen PL, Park YK. Apigenin and tt-farnesol with fluoride effects on S. mutans biofilms and dental caries. J Dent Res. 2005;84:1016-20.
• 47- Krcmery K Jr. Torupsis glabrata - an emerging yeast pathogen in cancer patients. Int J Antimicrob Agents. 1999;11:1-6.
• 48- Krcmery V, Barnes AJ. Non-albicans Candida spp. causing fungaemia: pathogenicity and antifungal resistance. J Hosp Infect. 2002;50:243-60.
• 49- Kulak Y, Kadir T. In vitro study of fungal presence and growth on three tissue conditioner materials. J Marmara Univ Dent Fac. 1997;2:682-4.
• 50- Kulak Y, Kazazoglu E. In vivo and in vitro study of fungal presence and growth on three tissue conditioning materials on implant supported complete denture wearers. J Oral Rehabil. 1998;25:135-8.
• 51- Kumamoto CA, Vinces MD. Alternative Candida albicans lifestyles: growth on surfaces. Annu Rev Microbiol. 2005;59:113-33.
• 52- Lamfon H, Porter SR, McCullough M, Pratten J. Formation of Candida albicans biofilms on non-shedding oral surfaces. Eur J Oral Sci. 2003;111:465-71.
• 53- Lefebvre CA, Wataha JC, Cibirka RM, Schuster GS, Parr GR. Effects of triclosan on the cytotoxicity and fungal growth on a soft denture liner. J Prosthet Dent. 2001;85:352-6.
• 54- Li L, Redding S, Dongari-Batgtzoglou. Candida glabrata, an emerging oral opportunistic pathogen. J Dent Res. 2007;86:204-15.
• 55- Luo G, Samaranayake LP. Candida glabrata, an emerging fungal pathogen, exhibits superior relative cell surface hydrophobicity and adhesion to denture acrylic surfaces compared with Candida albicans APMIS. 2002;110:601-10.
• 56- MacPhail LM, Greenspan D, Dodd CL, Heinic GS, Beck C, Ekoku E. Association of fungal species with oral candidiasis in HIV infection. J Dent Res. 1993;72:353.
• 57- Masella RP, Dolan CT, Laney WR. The prevention of the growth of Candida on silastic 390 soft liner for dentures. J Prosthet Dent. 1975;33:250-7.
• 58- Matsuura T, Abe Y, Sato Y, Okamoto K, Ueshige M, Akagawa Y. Prolonged antimicrobial effect of tissue conditioners containing silver- zeolite. J Dent. 1997;25:373-7.
• 59- Maza JL, Elguezabal N, Prado C, Ellacuría J, Soler I, Pontón J. Candida albicans adherence to resin-composite restorative dental material: influence of whole human saliva. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2002;94:589-92.
• 60- McCabe JF. A polyvinylsiloxane denture soft lining material. J Dent. 1998;26:521-6.
• 61- McCourtie J, MacFarlane TW, Samaranayake LP. Effect of saliva and serum on the adherence of Candida species to chlorhexidine-treated denture acrylic. J Med Microbiol. 1986;21:209-13.
• 62- McFarland LV. Normal flora: diversity and functions. Microb Ecol Health Dis. 2000;12:193-207.
• 63- McMullan-Vogel CG, Jüde HD, Ollert MW, Vogel CW. Serotype distribution and secretory acid proteinase activity of Candida albicans isolated from the oral mucosa of patients with denture stomatitis. Oral Microbiol Immunol. 1999;14:183-9.
• 64- Mikelsaar M, Mandar R. Development of individual lactic acid microflora in the human microbial ecosystem. In: Salminen S, von Wright A, ed. Lactic Acid Bacteria. 1st ed. New York: Marcel Dekker; 1993. p.256-60.
• 65- Millsap KW, Bos R, van der Mei HC, Busscher HJ. Adhesion and surface-aggregation of Candida albicans from saliva on acrylic surfaces with adhering bacteria as studied in a parallel plate flow chamber. Antonie Van Leeuwenhoek. 1999;75:351-9.
• 66- Millsap KW, Bos R, van der Mei HC, Busscher HJ. Adhesive interactions between voice prosthetic yeast and bacteria on silicone rubber in the absence and presence of saliva. Antonie Van Leeuwenhoek. 2001;79:337-43.
• 67- Minagi S, Miyake Y, Inagaki K, Tsuru H, Suginaka H. Hydrophobic interaction in Candida albicans and Candida tropicalis adherence to various denture base resin materials. Infect Immun. 1985;47:11-4.
• 68- Moura JS, Silva WJ, Pereira T, Del Bel Cury AA, Rodrigues Garcia RC. Influence of acrylic resin polymerization methods and saliva on the adherence of four Candida species. J Prosthet Dent. 2006;96:205-11.
• 69- Mukherjee PK, Zhou G, Munyon R, Ghannoum MA. Candida biofilm: a well-designed protected environment. Med Mycol. 2005;43:191-208.
• 70- Nevzatoðlu EU, Ozcan M, Kulak-Ozkan Y, Kadir T. Adherence of Candida albicans to denture base acrylics and silicone-based resilient liner materials with different surface finishes. Clin Oral Investig. 2007;11:231-6.
• 71- Nikawa H, Hayashi S, Nikawa Y, Hamada T, Samaranayake LP. Interactions between denture lining material, protein pellicles and Candida albicans Arch Oral Biol. 1993;38:631-4.
• 72- Nikawa H, Iwanaga H, Kameda M, Hamada T. In vitro evaluation of Candida albicans adherence to soft denture-lining materials. J Prosthet Dent. 1992;68:804-8.
• 73- Nikawa H, Jin C, Hamada T, Makihira S, Kumagai H, Murata H. Interactions between thermal cycled resilient denture lining materials, salivary and serum pellicles and Candida albicans in vitro Part II. Effects on fungal colonization. J Oral Rehabil. 2000;27:124-30.
• 74- Nikawa H, Jin C, Makihira S, Hamada T, Samaranayake LP. Susceptibility of Candida albicans isolates from the oral cavities of HIV-positive patients to histatin-5. J Prosthet Dent. 2002;88:263-7.
• 75- Nikawa H, Yamamoto T, Hamada T, Rahardjo MB, Murata H, Nakanoda S. Antifungal effect of zeolite-incorporated tissue conditioner against Candida albicans growth and/or acid production. J Oral Rehabil. 1997;24:350-7.
• 76- Palkova Z, Vachova L. Life within a community: benefit to yeast long-term survival. FEMS Microbiol Rev. 2006;30:806-24.
• 77- Perdigon G, Fuller R, Raya R. Lactic acid bacteria and their effect on the immune system. Curr Issues Intest Microbiol. 2001:2:27-42.
• 78- Pereira-Cenci T, Cury AA, Cenci MS, Rodrigues-Garcia RC. In vitro Candida colonization on acrylic resins and denture liners: influence of surface free energy, roughness, saliva, and adhering bacteria. Int J Prosthodont. 2007;20:308-10.
• 79- Quirynen M, Marechal M, Busscher HJ, Weerkamp AH, Darius PL, van Steenberghe D. The influence of surface free energy and surface roughness on early plaque formation. An in vivo study in man. J Clin Periodontol. 1990;17:138-44.
• 80- Radfar L, Kleiner DE, Fox PC, Pillemer SR. Prevalence and clinical significance of lymphocytic foci in minor salivary glands of healthy volunteers. Arthritis Rheum. 2002;47:520-4.
• 81- Radford DR, Challacombe SJ, Walter JD. Denture plaque and adherence of Candida albicans to denture-base materials in vivo and in vitro Crit Rev Oral Biol Med. 1999;10:99-116.
• 82- Radford DR, Radford JR. A SEM study of denture plaque and oral mucosa of denture-related stomatitis. J Dent. 1993;21:87-93.
• 83- Radford DR, Sweet SP, Challacombe SJ, Walter JD. Adherence of Candida albicans to denture-base materials with different surface finishes.J Dent. 1998;26:577-83.
• 84- Ramage G, Tomsett K, Wickes BL, Lopez-Ribot JL, Redding SW. Denture stomatitis: a role for Candida biofilms. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2004;98:53-9.
• 85- Ramage G, Vandewalle K, Wickes BL, Lopez-Ribot JL. Characteristics of biofilm formation by Candida albicans Rev Iberoam Micol. 2001;18:163-70.
• 86- Samaranayake LP, MacFarlane TW. An in vitro study of the adherence of Candida albicans to acrylic surfaces. Arch Oral Biol. 1980;25:603-9.
• 87- Samaranayake LP. Candida krusei infections and fluconazole therapy. Hong Kong Med J. 1997;3:312-4.
• 88- Samaranayake LP. Oral mycoses in HIV infection. Oral Surg Oral Med Oral Pathol. 1992;73:171-80.
• 89- Samaranayake YH, Samaranayake LP. Experimental oral candidiasis in animal models. Clin Microbiol Rev. 2001;14:398-429.
• 90- Samaranayake YH, Samarnayake LP. Candida krusei: biology, epidemiology, pathogenicity and clinical manifestations of an emerging pathogen. J Med Microbiol. 1994;41:295-310.
• 91 - San Millán R, Elguezabal N, Regulez P, Moragues MD, Quindos G, Ponton J. Effect of salivary secretory IgA on the adhesion of Candida albicans to polystyrene. Microbiology. 2000;146:2105-12.
• 92- Schmidt-Westhausen AM, Bendick C, Reichart PA, Samaranayake LP. Oral candidosis and associated Candida species in HIV-infected Cambodians exposed to antimycotics. Mycoses. 2004;47:435-41.
• 93- Serrano-Granger R, Campo-Trapero J, Del Río-Highsmith J. In vitro study of the adherence of Candida albicans to acrylic resins: relationship to surface energy. Int J Prosthodont. 2005;18:392-8.
• 94- Sipahi C, Anil N, Bayramli E. The effect of acquired salivary pellicle on the surface free energy and wettability of different denture base materials. J Dent. 2001;29:197-204.
• 95- Snydman DR. Shifting patterns in the epidemiology of nosocomial Candida infections. Chest. 2003;123:500S-3S.
• 96- Tanida T, Ueta E, Tobiume A, Hamada T, Rao F, Osaki T. Influence of aging on candidal growth and adhesion regulatory agents in saliva. J Oral Pathol Med. 2001;30:328-35.
• 97- Tari BF, Nalbant D, Dogruman Al F, Kustimur S. Surface roughness and adherence of Candida albicans on soft lining materials as influenced by accelerated aging. J Contemp Dent Pract. 2007;8:18-25.
• 98- Taylor R, Maryan C, Verran J. Retention of oral microorganisms on cobalt-chromium alloy and dental acrylic resin with different surface finishes. J Prosthet Dent. 1998;80:592- 7.
• 99- ten Cate JM. Biofilms, a new approach to the microbiology of dental plaque. Odontology. 2006;94:1-9.
• 100- Thein ZM, Samaranayake YH, Samaranayake LP. In vitro biofilm formation of Candida albicans and non-albicans Candida species under dynamic and anaerobic conditions. Arch Oral Biol. 2007;52:761-7.
• 101- Ulusoy M, Ulusoy N, Aydin AK. An evaluation of polishing techniques on surface roughness of acrylic resins. J Prosthet Dent. 1986;56:107-12.
• 102- Vasilas A, Molina L, Hoffman M, Haidaris CG. The influence of morphological variation on Candida albicans adhesion to denture acrylic in vitro. Arch Oral Biol. 1992;37:613-22.
• 103- Veerman EC, van den Keybus PA, Vissink A, Nieuw Amerongen AV. Human glandular salivas: their separate collection and analysis. Eur J Oral Sci. 1996;104:346-52.
• 104- Verheyen CC, Dhert WJ, de Blieck-Hogervorst JM, van der Reijden TJ, Petit PL, de Groot K. Adherence to a metal, polymer and composite by Staphylococcus aureus and Staphylococcus epidermidis. Biomaterials. 1993;14:383-91.
• 105- Verran J, Maryan CJ. Retention of Candida albicans on acrylic resin and silicone of different surface topography. J Prosthet Dent. 1997;77:535-9.
• 106- Verran J, Motteram KL. The effect of adherent oral streptococci on the subsequent adherence of Candida albicans to acrylic in vitro J Dent. 1987;15:73-6.
• 107- Viscoli C, Girmenia C, Marinus A, Collette L, Martino P, Vandercam B, Doyen C, Lebeau B, Spence D, Krcmery V, De Pauw B, Meunier. Candidemia in cancer patients: a prospective, multicenter surveillance study by the Invasive Fungal Infection Group (IFIG) of the European Organization for Research and Treatment of Cancer (EORTC). Clin Infect Dis. 1999;28:1071-9.
• 108- Waltimo T, Tanner J, Vallittu P, Haapasalo M. Adherence of Candida albicans to the surface of polymethylmethacrylateE glass fiber composite used in dentures. Int J Prosthodont. 1999;12:83-6.
• 109- Wargo MJ, Hogan DA. Fungalbacterial interactions: a mixed bag of mingling microbes. Curr Opin Microbiol. 2006;9:359-64.
• 110- Waters MG, Willians DW, Jagger RG, Lewis MA. Adherence of Candida albicans to experimental denture soft lining materials. J Prosthet Dent. 1997;3:306-12.
• 111- Wood S R, Kirkham J, Marsh P D, Shore R C, Nattress B, Robinson C. Architecture of intact natural human plaque biofilms studied by confocal laser scanning microscopy. J Dent Res. 2000;79:21-7.
• 112- Wright PS. The effect of soft lining materials on the growth of Candida albicans J Dent. 1980;8:144-51.
• 113- Young T. Philosophical transactions of the Royal Society of London. 9^th ed. London 1805. 255p.

Publication Dates

• Publication in this collection
  19 May 2008
• Date of issue
  Apr 2008

History

• Accepted
  06 Feb 2008
• Reviewed
  01 Oct 2008
• Received
  22 Nov 2007