Comparative Analysis of Biofilm Formation on Materials Used for the Fabrication of Implant-Supported Prostheses

Abstract

The purpose of this study was to compare biofilm formation on materials used for the fabrication of implant-supported dental prostheses. Twenty discs (D=15 mm, H=3 mm) were fabricated from one of the following restorative materials: yttria tetragonal zirconia polycrystal (Y-TZP); commercially pure titanium (CP-Ti); or heat-cured polymethyl methacrylate (PMMA). Specimens were polished following standard protocols. A non-contact profilometer (NPFLEX, Bruker, UK) was used to assess the surface roughness of each disk; results were reported as R_a (µm). Five strains of Gram-negative bacteria frequently associated with peri-implantitis, Aggregatibacter actinomycetemcomitans, Candida. albicans, Porphyromonas gingivalis, Prevotella intermedia, and Tannerella forsythia, were cultured on hand-polished discs fabricated from heat-cured PMMA, Y-TZP, or CP-Ti to compare biofilm formation on each type of material. The results were reported as colony-forming units per milliliter (CFU/mL). One-way ANOVA and post hoc tests were used to compare surface roughness and bacterial colonization on the respective materials. Statistical significance was set at a = 0.05. Discs fabricated from Y-TZP had a significantly higher R_a value (350 ± 30 µm) than either PMMA, or CP-Ti discs. Discs fabricated from either Y-TZP and CP-Ti may exhibit less colonization by bacteria associated with peri-mucositis and peri-implantitis. Y-TZP and CP-Ti are suggested materials for fabrication of implant-supported prostheses, considering biofilm formation.

Key Words:
biofilm formation; implant dentistry; zirconia; titanium; poly methyl methacrylate; peri-implantitis

Resumo

O objetivo deste estudo foi comparar a formação de biofilme em materiais utilizados na confecção de próteses dentárias implantossuportadas. Vinte discos (D = 15 mm, H = 3 mm) foram confeccionados com um dos seguintes materiais restauradores: zircônia tetragonal policristalina estabilizada por ítrio (Y-TZP); titânio comercialmente puro (CP-Ti); ou polimetilmetacrilato (PMMA). As amostras foram polidas seguindo protocolos padrão. Um perfilômetro sem contato (NPFLEX, Bruker, UK) foi usado para avaliar a rugosidade da superfície de cada disco; os resultados foram relatados como R_a (µm). Cinco cepas de bactérias Gram-negativas freqüentemente associadas a peri-implantite, Aggregatibacter actinomycetemcomitans, Candida. albicans, Porphyromonas gingivalis, Prevotella intermedia e Tannerella forsythia, foram cultivadas em discos polidos à mão feitos de PMMA, Y-TZP ou CP-Ti para comparar a formação de biofilme em cada tipo de material. Os resultados foram relatados como unidades formadoras de colônias por mililitro (UFC/mL). Análise de variância a um fator e testes post hoc foram usados ​​para comparar a rugosidade da superfície e a colonização bacteriana nos respectivos materiais. A significância estatística foi estabelecida em a=0,05. Os discos feitos de Y-TZP tiveram um valor R_a significativamente mais alto (350 ± 30 µm) do que os discos de PMMA ou CP-Ti. Os discos fabricados com Y-TZP e CP-Ti podem apresentar menor colonização por bactérias associadas à perimucosite e peri-implantite. Considerando O Y-TZP e CP-Ti são materiais indicados para a confecção de próteses implantossuportadas, considerando a formação de biofilme

Introduction

The physical and chemical traits, including surface free energy, roughness, and chemical composition of a material determine how robustly bacteria adhere to that substrate ^1,2,3. Given that bacterial biofilms, which form on restorative materials used in dental prostheses, have been strongly linked to the development of peri-mucositis and peri-implantitis, an understanding of the factors that promote bacterial adherence and growth is essential to provide positive patient outcomes. Therefore, in addition to considering the durability and esthetic qualities of a restorative material, identifying factors that increase the adherence of biofilm to a prosthesis may impact the long-term success of dental implants ⁴. For example, in vitro studies show that, when comparing multiple factors, an increased surface roughness has the greatest positive correlation with the amount of bacterial colonization and in determining the strain composition of dental biofilms ^5,6,7,8,9

Peri-mucositis and peri-implantitis associated with dental implants have similar characteristics with destructive periodontal diseases that occur around natural dentition. Both diseases are multifactorial and strongly correlated with the presence of gram-negative anaerobic bacteria in the microbiota surrounding the prostheses or natural dentition. These bacterial pathogens include Porphyromonas gingivalis, Treponema denticola, Tannerella forsythia, Fusobacterium species, and Prevotella intermedia ^{10,11,12,13,14,15,16,17}; additionally, the presence of Aggregatibacter actinomycetemcomitans, Staphylococcus aureus, and Candida albicans has also been reported at sites of peri-implantitis ^{18,19,20,21,22}.

The use of zirconia abutments and dental implants has significantly reduced irritation at the interface between the prosthesis and the peri-implant soft tissue ²³. Furthermore, multiple in vivo and in vitro investigations of the soft tissue response around zirconia prostheses revealed a better healing response and reduced plaque adhesion on prostheses fabricated from zirconia compared to those composed of titanium ^{24,25,26,27,28}. However, dental practitioners restore implants with variety of materials, including zirconia and other dental ceramic, heat-cured polymethyl methacrylate, titanium and other metal alloys, or a combination of these materials ^29,30,31. While durability and esthetics are important factors when choosing a material for implant supported prostheses, selecting restorative materials that are refractory to bacterial colonization will decrease the incidence of peri-implantitis.

This study compared both the surface roughness (R_a) of materials frequently used for the fabrication of definitive implant-supported prosthesis and the adherence of gram-negative anaerobic bacteria associated with peri-implantitis to these materials.

Material and Methods

Twenty discs using heat-cured polymethyl methacrylate (PMMA) (Lucitone 199; Dentsply; York, PA, USA), yttria tetragonal zirconia polycrystal (Y-TZP) (Zenostar; Ivoclar Vivadent; Amherst, NY, USA), or commercially pure titanium (CP-Ti) (Ti-6Al-4V, Staub Inc; Hamburg, NY, USA) were fabricated, for a total of sixty discs. All specimens were polished following the standard protocol described in Table 1 for the corresponding material. Next, to simulate clinical circumstances, all specimens were hand polished using an electric handpiece (NSK X20L 1:1; Brasseler USA; Savannah, GA, USA); polishing burs were used at 10,000 RPM.

Table 1
Restorative materials and polishing protocols

Material	Polishing protocol
CP-Ti	Machined CP Ti discs were polished for 20 s using a metal polishing kit with coarse-to-fine wheels (Airflex, Brasseler USA, Savannah, GA, USA)
Y-TZP	Milled Y-TZP discs were polished for 20 s using a Y-TZP polishing kit with coarse-to-fine wheels (Dialite ZR, Brasseler USA, Savannah, GA, USA)
PMMA	1: Processed PMMA discs were finished using 200-600 grit sandpaper: 2: Pumice slurry polishing for 20 s; 3: Acrylic polishing system for 20 s (medium to fine grit - Provisional Polisher, Brasseler USA, Savannah, GA, USA)

• PMMA=Heat-cured polymethyl methacrylate; Y-TZP=Yttria tetragonal zirconia polycrystal, CP-Ti=Commercially pure titanium.

Five discs fabricated from each material described above were chosen randomly for surface roughness assessment. After the polishing procedure, discs were placed in an ultrasonic cleaner containing distilled water for five minutes. Surface roughness (Ra) was measured by applying a non-contact profilometer (NPFLEX, Bruker, UK) to each specimen at four random regions of 1 mm by 1 mm in size. The surface roughness for each disc was determined by the averaging the Ra values found for each of the four measured regions.

After the assessment of surface roughness, discs were placed in an ultrasonic cleaner containing isopropyl alcohol for 10 min to remove debris. Specimens were then sterilized with ethylene oxide as specified by ISO 11135:2014 requirements for medical devices. Five strains of Gram-negative bacteria frequently associated with peri-implantitis ²⁴, A. actinomycetemcomitans (Aa), C. albicans (Ca), P. gingivalis (Pg), P. intermedia (Pi), and T. forsythia (Tf) were used in this study. Cryopreserved bacterial strains were used to inoculate non-selective blood agar media and incubated under anaerobic conditions for 72 h at 37 °C to allow bacterial growth. A bacterial colony from each strain was then used to inoculate brain-heart infusion (BHI) media and cultures were grown to an optical density (OD) of 0.5; the optical density was measured using a spectrophotometer (SmartSpec™3000, BIO-RAD; Hercules, CA, USA). The bacterial cultures were diluted ten-fold with BHI, dispensed onto the prepared Y-TZP, PMMA, or CP-Ti discs, and then incubated for 72 h under anaerobic conditions.

Next, to quantify the amount of bacterial growth on each disc, the number of colony-forming units were determined. Following incubation, discs were gently rinsed with distilled water to remove non-adherent bacteria, placed in an Eppendorf tube containing 1 mL volume of sterile Ringer’s solution, and held on a vortex mixer for 60 s to remove adherent bacteria from the discs. Using a spiral plater (Autoplate™4000, Spiral Biotech; Norwood, MA), petri dishes containing non-selective blood agar media were inoculated with undiluted 50 µL aliquots from each sample; plates were then incubated for 72 h at 37°C to allow bacterial growth. Bacterial colonies were counted and reported as CFU/mL according to manufacturer’s instructions (Autoplate™4000).

One-way ANOVA was followed by Tukey HSD, Game-Howell, or multiple comparison tests, which were used to statistically analyze the influence of material choice and surface roughness values on the amount of bacterial colonization, with statistical significance at a=0.05.

Results

For each material used, the mean surface roughness (R_a) values and standard deviations are presented in Table 2. Discs fabricated from either heat-cured PMMA or CP-Ti had significantly smaller R_a values than Y-TZP discs (p<0.05). However, there was no significant difference between the R_a values found for PMMA and CP-Ti discs (p>0.05).

Table 3 shows the average number of colony forming units (CFU/mL) for each bacterial strain and the corresponding material on which growth occurred. For Pi, Pg, and Aa, the equal variance assumption was not met (p=0.05); therefore, the Brown-Forsythe robust one-way ANOVA was used, followed by the Games-Howell test procedure. The equal variance assumption was met for Ca and Tf; therefore, results from the standard one-way ANOVA and the Tukey multiple comparison procedure were reported.

Table 2
Mean ± SD surface roughness (R_a) in µm for each restorative material

Group	Ra (µm)
PMMA	218 ± 87a
Y-TZP	360 ± 40b
CP-Ti	170 ± 22a

• PMMA=Heat-cured polymethyl methacrylate; Y-TZP=Yttria tetragonal zirconia polycrystal, CP-Ti=Commercially pure titanium. Different letters indicate statistically significant difference (p<0.05).

Results from a Brown-Forsythe robust one-way ANOVA indicated a significant difference in the growth of Pi (F2, 4.68=11.63, p=0.015), Pg (F2, 4.99=189.24, p<0.005), and Aa (F2, 5.79=731.53, p<0.005) by restorative material. For Pi, multiple comparisons test indicated a trend towards significance for the difference in bacterial growth on Y-TZP compared to PMMA (p=0.055), and on PMMA compared to CP-Ti (p=0.053); however, there was no significant difference in the amount of growth on CP-Ti compared to Y-TZP. For Pi, the highest mean cell count was found for PMMA, followed by Y-TZP and CP-Ti. For Pg, multiple comparisons test indicated a significant difference among all mean pairs (p<0.005). For Pg, the greatest number of colony-forming units was found for PMMA, followed by CP-Ti and Y-TZP, respectively. For Aa, a post hoc multiple comparisons indicated a significant difference between bacterial growth on Y-TZP compared to both PMMA (p<0.005) and CP-Ti (p<0.005); however, there was no significant difference in the amount of growth on PMMA compared to CP-Ti. For Aa, the highest mean cell count was found for PMMA, followed by CP-Ti and Y-TZP, respectively (Table 3).

Table 3
Mean ± SD number of colony forming units per milliliter for each bacterial strain adhered to PMMA, Y-TZP, or CP-Ti discs

Bacterial strain	PMMA	Y-TZP	CP-Ti
Pi	235185 ± 54328	134722 ± 29333	125000 ± 5345.83
Pg	174074 ± 13940.23	46401 ± 6779	107407± 4276
Aa	8333333 ± 427666	1079545 ± 196823	7777777 ± 213833
Tf	109722 ± 20697	22443 ± 4233	30397 ± 5756
Ca	17897 ± 1429	14015 ± 2531	26325 ± 4335

• Pi=Prevotella intermedia; Pg= Porphyromonas gingivalis; Aa=Aggregatibacter actinomycetemcomitans; Tf=Tannerella forsythia; Ca=Candida albicans; PMMA=Heat-cured polymethyl methacrylate; Y-TZP=Yttria tetragonal zirconia polycrystal; CP-Ti=Commercially pure titanium.

One-way ANOVA results indicated a significant difference in the growth of Tf growth (F2, 9=58.29, p<0.005) compared with Ca (F2, 9=17.44, p=0.001) by restorative materials. Multiple comparisons test indicated a significant difference between the amount of Tf found on PMMA compared to both Y-TZP (p<0.005) and CP-Ti (p<0.005); however, there was no significant difference between the amount of growth on Y-TZP compared to CP-Ti. For Tf, the highest mean cell count was found for PMMA, followed by CP-Ti and Y-TZP, respectively. For Ca, Multiple comparisons test indicated a significant difference between the amount of bacterial growth on CP-Ti compared to both PMMA (p=0.008) and Y-TZP (p=0.001); however, there was no significant difference between PMMA and Y-TZP. For Ca, the highest mean cell count was found for CP-Ti, followed by PMMA and Y-TZP, respectively (Table 3).

Discussion

This study evaluated the amount of bacterial colonization on three restorative dental materials routinely used for definitive implant-supported prostheses. Studies regarding bacterial adhesion to dental materials have shown that there is a direct positive correlation between the surface roughness of a substrate and bacterial adhesion to that material ^25,26,32. In this study, Y-TZP surface roughness was significantly higher than CP-Ti; however, Y-TZP discs exhibited either a similar, or significantly less (p<0.05), amount of bacterial colonization compared to CP-Ti discs. In addition to the surface roughness, there is a positive correlation between the wettability of a material and bacterial colonization ^32,33,34 Therefore, while Y-TZP has a higher surface roughness than CP-Ti, the lower wettability of Y-TZP compared to CP-Ti may have led to the comparable level of bacterial colonization on these materials that was observed in this study ³⁵.

This study found that Y-TZP discs had a greater surface roughness than PMMA discs, but this difference was not statistically significance. However, bacterial colonization was significantly higher for PMMA discs as compared to Y-TZP discs. This result may be due to the surface wettability or porous nature of PMMA compared to Y-TZP ³⁵.

Van Brakel et al. ³³ evaluated early bacterial colonization of zirconia and titanium abutments; however, no statistically significant difference was observed in the growth of several indicator bacteria, including A. actinomycetemcomitans, P. gingivalis, P.intermedia, and T. forsythia, between the zirconia and titanium abutments. Similarly, in a study that examined colonization by A. actinomycetemcomitans and P. gingivalis, Salihoglu et al. ³⁶ found that Y-TZP discs had similar, or significantly less, bacterial colonization levels as compared to CP-Ti discs. The difference in our results may be a result of differences in the surface roughness of the specimens; Van Brakel et al. ³³ evaluated discs with considerably larger Ra values (210-236 nm), while the Ra values in this study were much lower. However, the Ra value was not reported in the study performed by Salihoglu et al ³⁶.

Although there are studies evaluating materials for implant-supported crowns; previous studies have not evaluated colonization of PMMA compared to Y-TZP and CP-Ti by bacteria associated with peri-implantitis. These materials are used individually, or in combination, for the fabrication of implant-supported prosthesis. This study found a higher level of bacterial colonization on PMMA discs as compared to CP-Ti and Y-TZP discs. This result may be due to the porous nature of heat-cured PMMA and the associated surface energy ³⁷.

The outcome of this study suggests that implant-supported prosthesis fabricated from Y-TZP with or without CP-Ti might be a superior prosthetic option for fewer bacteria colonization. However, future studies should include additional materials such as CAD-CAM fabricated PMMA.

The present study shows that bacteria colonize Y-TZP to a similar, or lesser, extent compared to CP-Ti; these results suggest that use of Y-TZP restorations may result in a similar, or fewer, number of peri-mucositis and peri-implantitis cases. Additionally, as compared to restorations fabricated from Y-TZP and CP-Ti, our results suggest that the use of heat-cured PMMA in dental prostheses may lead to an increased colonization by bacteria associated with peri-mucositis and peri-implantitis.

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Publication Dates

• Publication in this collection
  04 Sept 2020
• Date of issue
  Jul-Aug 2020

History

• Received
  17 Jan 2020
• Accepted
  20 Apr 2020