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. 2024 Oct 16;36(12):1539–1543. doi: 10.1016/j.sdentj.2024.10.001

Adhesion of Candida albicans on preformed crowns used to restore primary molars: An in vitro study

Eman A Bakhurji a,⁎, Doaa M AlEraky b, Hend Alshammary c, Marwah Alamoudi c, Nabras Alrayes c, Mohamed Hassan d
PMCID: PMC11976092  PMID: 40952874

Abstract

Background

Assessing microbial biofilm adhesion to the restorative material’s surface is a key factor in determining its success. This study aimed to compare the adhesion of Candida albicans (C. albicans) on stainless steel crowns (SSCs) versus zirconia crowns (ZCs) used for primary molars.

Study design

This in vitro study involved 20 full-coverage crowns, with 10 SSCs and 10 ZCs. A fungal adhesion assay was performed to evaluate C. albicans adhesion, using colony-forming units (CFU) and cell proliferation assays.

Statistics

The Wilcoxon–Mann–Whitney test was applied to compare the groups, with statistical significance set at 5 %.

Results

The study revealed that SSCs had a lower mean CFU value (28.28 ± 4.557 CFU/ml) and cell proliferation rate (49.74 ± 0.4367) compared to the ZC group (30.70 ± 11.0760 CFU/ml and 74.53 ± 0.7014, respectively). However, these differences were not statistically significant.

Conclusion

The findings suggest that the selection of crowns for restoring primary molars may not be influenced by C. albicans adhesion.

Keywords: Stainless steel crowns, Zirconia crowns, CFU, Biofilm adhesion, Cell proliferation assay

1. Introduction

Primary teeth play a vital role in the growth and development of children's dentition. [Abdulhadi et al., 2017, AlShaibah et al., 2012, Wakwak et al., 2019] To preserve primary teeth until the eruption of permanent teeth, various restorative materials and techniques have been developed. [Abdulhadi et al., 2017, Gurunathan et al., 2021, Wakwak et al., 2019] Since Humphrey introduced stainless steel crowns (SSCs) for pediatric patients in 1950, they have remained one of the most widely used restorative options. [AlShaibah et al., 2012, Wakwak et al., 2019, Suguna and Gurunathan, 2021, Mathew et al., 2020a, Seale and Randall, 2015] Research indicates that SSCs outperform amalgam and other tooth-colored restorations in the treatment of multisurface cavities, cervical decalcification, and developmental defects. [AlShaibah et al., 2012, Wakwak et al., 2019, Suguna and Gurunathan, 2021, Mathew et al., 2020a] Compared to other restorative options, SSCs offer greater longevity and cost-effectiveness. [Abdulhadi et al., 2017, Randall, 2002] Additionally, SSCs have a lifespan comparable to that of a healthy primary tooth and protect the remaining tooth structure, which may be compromised after extensive caries removal. [Wakwak et al., 2019, Abdulhadi et al., 2017] The primary advantage of SSCs is their reduced technique sensitivity, making them a more favorable option when treating pediatric patients. [Wakwak et al., 2019] However, their lack of aesthetic appeal is a major drawback in cases with high aesthetic requirements. [AlShaibah et al., 2012, Suguna and Gurunathan, 2021] This limitation led to the development of more aesthetic alternatives, such as pre-veneered SSCs, strip crowns, and zirconia crowns (ZCs). [Suguna and Gurunathan, 2021, Mathew et al., 2020b] Although pre-veneered SSCs offer improved aesthetics, their increased bulkiness poses a problem, leading to a higher incidence of gingival inflammation. [AlShaibah et al., 2012, Abdulhadi et al., 2017] In 2008, Sprig Oral Health (formerly EZ Pedo) (Sprig Oral Health Technologies, Inc., Loomis, CA, USA) introduced ZCs to pediatric dentistry, offering a solution that combines aesthetic appeal, biocompatibility, and enhanced mechanical strength [AlShaibah et al., 2012, Abdulhadi et al., 2017].

Evaluating microbial biofilm adhesion on restorative material surfaces is a key factor in determining the material's success because it is the first stage of microbial colonization. [AlShaibah et al., 2012, Beldüz et al., 2017, Randall, 2002, Zupancic Cepic et al., 2020] In terms of preventing plaque adhesion, ZCs have shown superior performance compared to SSCs. [Wakwak et al., 2019] Previous studies assessed the adhesion of Streptococcus mutans and Lactobacillus on both SSCs and ZCs, consistently reporting significantly higher adhesion on SSCs than on ZCs. [Wakwak et al., 2019, Mathew et al., 2020b, Suguna and Gurunathan, 2021] Additionally, Candida albicans (C. albicans) is significantly associated with early childhood caries (ECC), with children harboring C. albicans being over five times more likely to develop ECC compared to those without it. [Xiao et al., 2018] However, no studies have yet assessed C. albicans adhesion on SSCs and ZCs. Thus, the aim of this study was to evaluate the initial adhesion and mature biofilm formation of C. albicans on SSCs versus ZCs used for primary molars.

2. Materials and methods

2.1. Study design

This in vitro experimental investigation was performed in a microbiology research lab and did not involve any human participants or tissues. All procedures adhered to relevant laws and institutional guidelines, with approval granted by the Institutional Review Board at the Deanship of Scientific Affairs (ethical approval #2022-02-378). The study protocol followed the Checklist for Reporting in Vitro Studies (CRIS) guidelines for laboratory research not involving human tissues.

2.2. Sample size calculation

The sample size was calculated using a non-inferiority test based on a previous study. [AlShaibah et al., 2012], which investigated the mean difference and standard deviation in Streptococcus mutans adhesion between SSCs (44.16 ± 5.7) and ZCs (2.43 ± 2.3). With an 80 % power, a 95 % confidence interval, and a minimum detectable effect of 3, the required sample size was determined to be 7 crowns per group. However, this was increased to 10 crowns per group to account for potential laboratory errors.

2.3. Specimen preparation

For this study, we utilized 10 SSCs and 10 ZCs (©2021 NuSmile Ltd., Houston, TX, USA) of size E3. We divided the specimens into two equal groups (Fig. 1) and sterilized them at 121 °C for 20 min following the manufacturer's instructions.

Fig. 1.

Fig. 1

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Flowchart of the study groups.

2.4. Preparation of C. albicans suspension

C. albicans was obtained from the American Type Culture Collection (ATCC reference strain ATCC 90028) and was used throughout the study, stored as a glycerol stock at −80 °C. We prepared Sabouraud dextrose agar (denoted SDA) as well as Sabouraud dextrose broth (denoted SDB) culture media for each group by following the instructions provided by the manufacturer. Before each experiment, C. albicans reference strains were incubated on SDA at 37 °C for 48 h. The microbial broth was prepared, and its turbidity was adjusted to 0.5 McFarland's solution (1 × 108 colony-forming units (CFU)/mL), yielding approximately 1 × 106 CFU/mL, using the DensiCHEK (BioMérieux Inc, France).

2.5. Fungal adhesion assay

Each specimen was placed in a 12-well tissue culture plate with the interior surface of the crowns facing upward to prevent yeast overgrowth on the fitting surface. To allow us to measure the biofilm formation, we added 1000 μL of yeast cell suspension. Next, we incubated the plate for 48 h using the temperature of 37 °C. Following incubation, we transferred the specimens to a clean plate and rinsed them with 2 mL of phosphate-buffered saline (PBS; pH 7.0) to eliminate non-adherent cells. The adherent Candida cells were then removed from the surfaces of the specimens by vortexing in PBS (1-mL volume) for a duration of 5 min.

2.6. Colony-forming unit (CFU) assay

A volume of 100 µL of the cell suspension was spread onto SDA agar using a sterile cotton applicator. Colony-forming unit (CFU) counts were determined after 48 h of incubation at 37 °C. The CFU counts (CFU/mL) of C. albicans were recorded using the online digital colony counter application “APD Colony Counter App PRO,” with validation through conventional manual counting methods. [Michael et al., 2022] The number of adherent viable cells was expressed as CFU/mL.

2.7. Cell proliferation assay

A kit designed for counting cells (specifically, CCK-8/WST-8) (ab228554, Abcam, Waltham, MA, USA), utilizing monosodium salt WST-8, was employed to quantify live cells, according to the guidelines provided by the manufacturer. From each sample, we transferred 100 µL of adherent cell suspensions to a reaction plate containing 96 wells. Then, we added 10 µL of dye to each well. Following a 3-h incubation under dark conditions at 37 °C, the cellular dehydrogenases generated a soluble orange formazan product. [Kwolek-Mirek and Zadrag-Tecza 2014] In the WST-8 kit, cells that are metabolically active reduce the salt, producing an orange-colored formazan product that can be quantified with a plate reader spectrophotometer. Color intensity directly indicates the presence of metabolically active or live cells and their proliferation. [Kwolek-Mirek and Zadrag-Tecza 2014] A microplate reader (Bio-Rad xMark™ Microplate Spectrophotometer, Hercules, CA, USA) was used to measure the absorbance of the cell suspension at 490 nm. The generation of formazan is directly linked to the quantity of viable cells [Kwolek-Mirek and Zadrag-Tecza 2014].

2.8. Statistical analysis

Descriptive statistics, such as mean as well as standard deviation, were employed to calculate the adhesion values of C. albicans isolates for SSCs and ZCs using IBM SPSS Statistics 28.0. The Wilcoxon–Mann–Whitney test was performed to compare C. albicans adhesion between the two types of crowns, with a significance level set at 5 %. We plotted the results using specialized software (specifically GraphPad Prism 8) developed by GraphPad Software, Inc., La Jolla, CA, USA.

3. Results

A total of 20 crowns (10 SSCs and 10 ZCs) were tested for Candida adhesion. CFUs were counted for both the 10 ZC and 10 SSC samples. The experiment was repeated twice for the cell proliferation assay, resulting in 40 crown samples, equally distributed between the two groups. Fig. 1 depicts the distribution of the study groups.

The overall mean CFU counts for ZCs were 30.70 ± 11.0760 CFU/mL ± SD × 102, while the overall mean for SSCs was 28.28 ± 4.557 CFU/mL ± SD × 102. The combined mean for both ZCs and SSCs was 29.55 ± 8.28; however, the results did not show statistical significance (p-value > 0.05). Fig. 2 (A) depicts the evaluation results of the mature biofilm adhesion assay.

Fig. 2.

Fig. 2

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Results of the biofilm assay.

The overall mean cell proliferation assay for ZCs was 74.53 ± 0.70136, while the mean for SSCs was 49.74 ± 0.43666. The analysis indicated that the results between the study groups were not statistically significant, with a p-value > 0.05. Fig. 2 (B) shows the results of the cell proliferation assay. The findings from both the CFU and cell proliferation assays are comparable. Table 1 summarizes the results of both experiments.

Table 1.

Mean, standard deviation (SD), and significance of the cell proliferation assay and colony-forming units (CFUs) (CFU/mL).

ZC (N = 10) SSC (N = 10)
Cell Proliferation Mean absorbance ± SD
74.5 ± 0.70 49.7 ± 0.44
p-value 0.74
ZC (N = 10) SSC (N = 10)
Colony Forming Unit Mean CFU/mL ± SD × 102
30.7 ± 11 28.28 ± 4.67
p-value 0.63
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4. Discussion

Microbial plaque adhesion considerably contributes to the initiation and progression of dental caries and periodontal disease in primary teeth. [Lobo et al., 2019] C. albicans and other Candida species are known for their biofilm formation, which is a key virulence factor. Additionally, these biofilms can be challenging to remove, especially given the emerging antifungal resistance associated with commonly used antifungal agents. [Seneviratne et al., 2008, Atiencia-Carrera et al., 2022b] Furthermore, these fungal infections can invade the host's immune system and change the host's immune response. [Cangui-Panchi et al., 2023] Conversely, the surface properties of restorative materials—such as surface characteristics, texture, area, and smoothness—directly influence the level of microbial adhesion, colonization, and aggregation. [Mathew et al., 2020a] C. albicans has been linked to early childhood caries (ECC) and various forms of active dental caries. [de Carvalho et al., 2006, Sziegoleit et al., 1999, Ugun-Can et al., 2007, Ghasempour et al., 2011] Therefore, developing strategies to reduce C. albicans counts in the oral cavity would considerably benefit the oral health of pediatric patients. This is particularly relevant for medically compromised patients and those at high risk for caries. [Kamagata-Kiyoura et al., 2003] Patients with systemic diseases that reduce salivary flow are more prone to Candida adhesion owing to saliva's diminished ability to detach fungal colonies. [Kamagata-Kiyoura et al., 2001, Torres et al., 2002, Mohammadi et al., 2016, Khan et al., 2014] Individuals undergoing chemotherapy, radiation therapy, or organ transplants face a higher risk of oropharyngeal and systemic spread of C. albicans owing to weakened immunity. Additionally, children with systemic conditions such as diabetes, congenital or cyclic neutropenia, or Human Immunodeficiency Virus (HIV) are at increased risk of developing systemic C. albicans infections owing to their compromised immune systems.

Techniques that evaluate yeast cell growth in various media (solid or liquid) are frequently employed in assessing the viability of cells, with CFUs typically utilized to quantify colony numbers. [Khattar et al., 2023] The starting cell concentration in an assay containing biofilm considerably affects the characteristics of the resulting biofilms. However, CFU assays may not provide an accurate estimate of viable yeast cells or those that are incapable of reproducing. A recent study indicated that the crystal violet assay showed a similar correlation with CFU counting and performed better than the LIVE/DEAD Biofilm Viability kit. [Atiencia-Carrera et al., 2022a] However, it is a simple and cost-effective method for assessing growth levels. In our study, we assessed C. albicans adhesion based on cell counting, employing dye staining-based kits (CCK-8/WST-8), which provide a more accurate estimate of cell death rates. [Khattar et al., 2023] Previous research has shown that using CCK-8/WST-8 to evaluate biofilm formation in the studied C. albicans strains is the most dependable, precise, and feasible method. [Khattar et al., 2023] Because both CFU assays and kits relying on cell counting (such as CCK-8 and WST-8) may lack accuracy and reliability individually, using both methodologies in conjunction is advisable.

Previous studies have examined the differences in bacterial adhesion between SSCs and ZCs, revealing significant differences between the two groups. [Wakwak et al., 2019, Mathew et al., 2020b, Suguna and Gurunathan, 2021] However, our study showed that the difference in adhesion of C. albicans was not significant between the studied groups. A potential explanation for this lack of significant difference may be the unique adhesion characteristics exhibited by C. albicans compared to bacteria and other Candida species. [Ramage et al., 2005, Kuhn et al., 2002] The initial adhesion of C. albicans begins after 30 min, followed by cell division, proliferation, and the formation of a mature biofilm in 24–48 h. [Rodríguez-Arias et al., 2022, Ramage et al., 2005] This mature biofilm is characterized by a dense network of yeasts, hyphae, and pseudohyphae. [Ramage et al., 2005] A unique feature of C. albicans related to its pathogenicity is morphogenetic conversion, allowing the organism to switch between hyphal and filamentous forms that facilitate its pathogenic adhesion. [Brown et al., 2007, Gow et al., 2002] The hyphal form of Candida is crucial for maintaining the structural integrity of the mature biofilm. [Baillie and Douglas, 1999] Additionally, filamentation considerably contributes to the establishment of a multilayered and well-structured biofilm. [Ramage et al., 2002] A study investigating biofilms formed by C. albicans mutants that are unable to filament revealed that these mutants produced poor-quality biofilms, lacking the complexity and integrity found in biofilms generated by filamenting C. albicans. [Ramage et al., 2002] Compared to bacteria, the complexity of the biofilms produced by C. albicans, along with its unique virulence factors, may be the reason for its adhesion on both SSCs and ZCs regardless of the type of material.

While the results of this study suggest that the choice of crowns may not be influenced by C. albicans adhesion, further research is necessary to fully understand the interaction between C. albicans and crown materials. This understanding is essential for effectively integrating these findings into clinical practice.

5. Conclusion

Owing to the limitations of the performed study, we identified no significant differences in the microbial adhesion of C. albicans between SSCs and ZCs. The selection of a crown should be guided by the clinician's judgment, taking into account factors such as bacterial adhesion, aesthetic requirements, the patient's behavior, and socio-economic considerations. For patients with special care needs, the choice of crown may not be influenced by susceptibility to fungal infections.

Author contribution statement

Conceptualization; EB, DE, MH. Data curation; HA, MA, NA, DE. Formal analysis; EB, HA, MA, NA. Funding acquisition; Not applicable. Investigation; DE, HA, MA, NA. Methodology; DE, EB, MH. Project administration; EB, DE. Resources; DE, HA, MA, NA. Software; EB. Supervision; EB, DE. Validation; MH. Visualization; MH. Roles/Writing − original draft; HA, MA, NA, MH. Writing − review & editing; EB, DE, MH. EB, DE, HA, MA, NA, MH: approval of final version of the manuscript.

Ethical approval

All procedures were performed in compliance with relevant laws and institutional guidelines and have been approved by The Institutional Review Board at the Deanship of Scientific Affairs (ethical approval #2022-02-378).

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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