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Remineralization of early enamel caries lesions using different bioactive elements containing toothpastes an in vitro study pdf

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22 METHODS: Artificial carious lesions were created on 40 human enamel slabs, and were randomly divided into four groups: 1 23 control group no treatment, 2 casein phosphopeptide-amorpho

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Remineralization of early enamel caries

1

lesions using different bioactive elements

2

containing toothpastes: An in vitro study

3

Yu Wanga, Li Meib, Lin Gonga, Jialing Lic, Shaowei Hed, Yan Jiaand Weibin Sune,∗

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aDepartment of Preventive Dentistry, Nanjing Stomatological Hospital, Medical School of Nanjing

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University, Nanjing, Jiangsu, China

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bDiscipline of Orthodontics, Department of Oral Science, Faculty of Dentistry, University of Otago,

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Dunedin, New Zealand

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cDepartment of Orthodontics, Institute and Hospital of Stomatology, Nanjing University Medical

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School, Nanjing, Jiangsu, China

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dDepartment of Prosthodontics, Nanjing Stomatological Hospital, Medical School of Nanjing

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University, Nanjing, Jiangsu, China

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eDepartment of Periodontics, Nanjing Stomatological Hospital, Medical School of Nanjing University,

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Nanjing, Jiangsu, China

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Received 22 November 2015

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Accepted 28 April 2016

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Abstract.

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BACKGROUND: Demineralization can be arrested or reversed when remineralization agents are applied to incipient carious

18

or non-cavitated carious lesions A large number of therapeutic agents including non-fluoridated products have been developed

19

to promote enamel remineralization.

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OBJECTIVE: This study aims to evaluate the efficacy of different bioactive elements containing toothpastes in

remineraliza-21

tion of artificial enamel lesions.

22

METHODS: Artificial carious lesions were created on 40 human enamel slabs, and were randomly divided into four groups: (1)

23

control group (no treatment), (2) casein phosphopeptide-amorphous calcium phosphate group (CPP-ACP, GC Tooth Mousse),

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(3) 8% arginine and calcium carbonate group (ACC, Colgate Sensitive Pro-Relief), (4) calcium sodium phosphosilicate group

25

(CSP, NovaMinR) All samples were subjected to 15 days of pH-cycling Subsequently, a one-hour acid resistance test was

26

carried out Surface hardness of the samples was assessed using the Knoop hardness test, and surface morphology and

rough-27

ness were assessed by scanning electron microscopy (SEM) and atomic force microscopy (AFM) Data were analyzed using

28

one-way ANOVA, Tukey’s test and pairedt test.

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RESULTS: The three tested toothpastes exhibited a significantly higher remineralization efficacy compared with the control

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group (P < 0.05 for all) After pH-cycling, the specimens treated with Colgate Sensitive Pro-Relief and NovaMin R showed

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a significant higher surface hardness (P < 0.001 and P = 0.03, respectively) and lower surface roughness (P < 0.05 for

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both) compared those treated with GC Tooth Mousse While after the acid resistance test, all groups showed a significant loss

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of surface hardness (P < 0.001 for all) and significant increase of surface roughness (P < 0.05) The specimens treated with

34

Corresponding author: Weibin Sun, Department of Periodontics, Nanjing Stomatological Hospital, Medical School of

Nan-jing University, 30 Zhongyang Road, NanNan-jing, Jiangsu, China Tel.: +86 25 83620173; Fax: +86 25 82620173; E-mail: wbsun@ nju.edu.cn.

0928-7329/16/$35.00 c 2016 – IOS Press and the authors All rights reserved

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Colgate Sensitive Pro-Relief and NovaMinR still showed a significant higher surface hardness and lower surface roughness

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in comparison with those treated with GC Tooth Mousse (P < 0.05 for all) No significant difference was found in surface

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hardness and roughness between Colgate Sensitive Pro-Relief and NovaMinR during the pH-cycling test and acid resistance

37

test (P = 0.45 and P = 0.83, respectively).

38

CONCLUSIONS: Colgate Sensitive Pro-Relief and NovaMinR present an advantage in enhancing remineralization and

in-39

hibiting demineralization for early enamel carious lesions in comparison with GC Tooth Mousse.

40

Keywords: Bioactive elements, dental caries, hardness, pH-cycling, remineralization

41

1 Introduction

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Dental caries is a dynamically alternative process of demineralization and remineralization Dem-43

ineralization can be arrested or reversed when remineralization agents are applied to incipient carious 44

or non-cavitated carious lesions [1,2] Therefore, it is of great importance to explore novel strategies 45

and approaches to enhance the remineralization process Fluoride has been widely recommended as a 46

remineralization agent for preventing early enamel carious lesions [3] The cariostatic effects of fluo-47

ride are mostly topical to precipitate calcium fluoride minerals on the surface of enamel and bacterial 48

plaque [4] Such cariostatic therapeutic effects of fluoride are inadequate to deal with high caries risk 49

patients [5] Promising remineralization effects are possible using high fluoride concentration agents [6] 50

However, fluoride has a dose-response relationship, and careless handling of fluoride toothpastes may 51

lead to adverse effects such as fluorosis [7] Considering the clinical significance of remineralization, a 52

range of therapeutic agents including non-fluoridated products has been developed to enhance enamel 53

remineralization A few examples of widely used remineralization materials are casein phosphopeptide-54

amorphous calcium phosphate (CPP-ACP) and bioactive glasses

55

CPP-ACP is an amorphous calcium phosphate (ACP)-based bioactive material stabilized by casein 56

phosphopeptide (CPP) It stabilizes free calcium and phosphate ions along with fluoride ions in a 57

metastable solution to bind to pellicle and bacterial plaque As a reservoir of bioactive calcium and 58

phosphate ions [8], CPP-ACP delivers ions to the enamel subsurface, and enhances its remineralization 59

effectively [9,10] A number of studies [8,9] report the anticariogenic effects of CPP-ACP technology 60

The formation of the CPP-ACP nanocomplex or ACPF complex takes place when CPP-ACP interacts 61

with fluoride ions [11]

62

NovaMinR is another biomaterial that consists of sodium-calcium-phosphate particles, which can 63

be activated in an aqueous environment Sodium ions present in NovaMinR are rapidly released, and 64

calcium and phosphate ions precipitate to form a calcium phosphate layer This is followed by the forma-65

tion of a carbonate-enriched HCA layer [12] The incorporation of HCA and bioactive sodium-calcium-66

phosphate particles result in the remineralization of early enamel caries lesions [9,11,12]

67

Pro-ArginTM, a novel remineralization agent, is a saliva-based compound that contains arginine (8%) 68

and calcium carbonate; which has been introduced to relieve dentin hypersensitivity [13] Arginine and 69

calcium carbonate form positively charged agglomerates that readily bind to negatively charged dentin 70

surfaces or tubules, facilitating calcium and phosphate ions to precipitate on the dentin surface [14] 71

Arginine and calcium are two key components of toothpastes that work together to deposit a dentin-like 72

mineral layer within dentin tubules and on the dentin surface

73

The in vitro study was designed to evaluate the remineralization potential of various commercial

tooth-74

pastes that contain different active remineralization components

75

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Fig 1 Flowchart: (a) teeth were cut at the cementoenamel junction; (b) crowns were sectioned mesiodistally and buccolingually into four parts; (c) enamel windows were created in the middle one-third of the crown, and an artificial lesion was produced; (d) samples were processed for the Knoop microhardness test; (e) pH-cycling was conducted for 15 days; (f) samples were processed for the Knoop microhardness test after pH-cycling; (g) enamel slabs were subjected to one-hour acid resistance testing; (h) a Knoop microhardness test was carried out after acid resistance testing.

2 Materials and methods

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2.1 Specimen preparation

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Ten human permanent premolars extracted for orthodontic treatment were obtained from Nanjing 78

Stomatological Hospital All selected teeth were inspected under a stereomicroscope (ACT-1, Nikon, 79

Japan) at 100x magnification to ensure that all teeth are free of stains, decay or cracks Debris, soft 80

tissue remnants and calculus were removed ultrasonically; and teeth were stored in athymol solution 81

(0.01%) for 48 hours All teeth were dissected using a low-speed cutting saw (Isomet, Buheler, USA) at 82

the cementoename junction (Fig 1a) Each tooth crown was sectioned mesiodistally and buccoling ually 83

into four parts (Fig 1b) Each thus-prepared enamel sample was embedded in acrylic resins and polished 84

progressively using a 600-grit wet silicon-carbide paper Enamel windows were created (4× 5 mm) in

85

the middle one-third of the crown by coating the surrounding surfaces with acid-resistant nail varnish 86

(Fig 1c) All samples were stored in distilled water at 37C This research protocol was approved by the

87

Ethical Committee of Nanjing Stomatological Hospital, Medical School of Nanjing University, China 88

2.2 Experimental groups

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The enamel slabs (n = 40) were randomly divided into four groups (each group, n = 10): (1) Control

90

group (no treatment); (2) CPP-ACP group (GC Tooth Mousse, GC Corporation, Japan); (3) ACC group 91

(8% arginine and calcium carbonate; Colgate Sensitive Pro-Relief, Colgate-Palmolive Company, USA); 92

(4) CSP group (calcium sodium phosphosilicate; NovaMinR, Beijing Bio-Tech Co Ltd, China). 93

Slurries were prepared by stirring the above toothpastes in distilled water at a fixed ratio (1:3), as 94

previously described [15] Fresh slurries were prepared on the day of application, and centrifuged at 95

4,000 rpm for 20 minutes

96

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2.3 Artificial lesion formation

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Artificial carious lesions were created by exposing the enamel slabs to a demineralization solution 98

(2.2 mM of calcium chloride, 2.2 mM of potassium hydrogen orthophosphate, unstirred solution of 99

0.05 M of acetic acid, and 1 M of potassium hydroxide; pH4.5) at 37C for 96 hours (Fig 1c) Then,

100

specimens were washed thoroughly using a spray of water and air-dried

101

2.4 pH-cycling

102

Fifteen days of pH-cycling was carried out at 37C, which consisted of three hours of

demineraliza-103

tion, followed by immersion in a remineralization solution for two hours A second cycle was performed, 104

which consisted of three hours of demineralization and an overnight remineralization Specimens were 105

placed into the previously described dentifrice supernatant solution 60 seconds before the first deminer-106

alizing cycle, and both before and after the second demineralizing cycle (Fig 1e) All specimens were 107

stored in distilled water at 37C until required for further experimentation.

108

2.5 Acid resistance testing (ART)

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In order to assess acid resistance effects, all specimens were washed using deionized distilled water, 110

and immersed in a demineralization solution at 37C for one hour The demineralization solution was

111

refreshed after microhardness testing and before acid resistance testing (Fig 1g)

112

2.6 Surface microhardness measurement

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The Knoop surface hardness (KHN) of enamel specimens was measured using a digital microhardness 114

tester (HV-1000, Shangcai Tester Manufactory, China) A Knoop diamond indenter under a 100-gload 115

was used for 10 seconds An average of five indentations was used for analyzing each specimen (Figs 1d, 116

1f and 1h) Data were collected at the following stages: a) baseline (sound enamel); b) after demineral-117

ization; c) after pH-cycling; d) after acid resistance test

118

2.7 Scanning electron microscopy (SEM)

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SEM observation was carried out using a scanning electron microscope (S-3400N, Hitachi, Japan) to 120

investigate morphological changes Specimens were mounted on aluminum stubs with a carbon tape, 121

and sputter-covered with carbon

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2.8 Atomic force microscopy (AFM)

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AFM images of the enamel surface were obtained using a Dimension FastScan BioTMAtomic Force 124

Microscope (Bruker Corporation, USA), which was operated in Scan Asyst mode using silicon tips 125

Topography images were collected at a low scan rate, covering a 30µm × 30 µm area with a 256 × 256

126

pixel resolution In each image, five randomized boxes of 2µm × 2 µm were drawn using the Bruker

127

NanoScope Analysis (Bruker Corporation, USA) at the enamel surface, and mean roughness (Ra) values 128

were determined

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2.9 Statistical analysis

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Statistical analysis was performed using one-way ANOVA, Tukey’s test and Pairedt test.

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Table 1 Knoop hardness number of enamel blocks at different stages

310± 7b2

338± 11d3

242± 9g4

Colgate Sensitive Pro-Relief 371± 6a1

307± 7b2

355± 8e3

271± 13h4

304± 10b2

350± 7e3

262± 5h4

Same lowercase letter indicated no statistical difference in columns Same number indicated no statistical difference in rows (P < 0.05) DM, demineralization; RM, remineralization; ART, acid resistance testing.

Table 2 Comparison of KHN within groups

Baseline→ DM 17.03 < 0.001 18.21 < 0.001 32.63 < 0.001 16.67 < 0.001

DM, demineralization; RM, remineralization; ART, acid resistance testing.

Table 3 Multiple comparison of surface hardness (KHN) among groups at different stages

Group 1, control group; group 2,casein phosphopeptide-amorphous calcium phosphate (CPP-ACP) group; group 3, 8% arginine and calcium carbonate (ACC, Colgate Sensitive Pro-Relief) group; group 4, calcium sodium phosphosilicate (CSP, NovaMinR) group; MD, mean difference.

3 Results

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3.1 Knoop hardness (KHN)

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The baseline surface hardness (KHN) was similar among all groups (P > 0.05) (Table 1) After the

134

application of different dentifrices, the KHN values in the treatment groups (GC Tooth Mousse, Col-135

gate Sensitive Pro-Relief, and NovaMinR groups) were all significantly increased (P < 0.001) (338 ±

136

11,355± 8, and 350 ± 7, respectively) Following the acid resistance tests (ART), a significant

reduc-137

tion of KHN values was observed in all groups (Table 1) (P < 0.001) The changes of surface hardness

138

within each group are summarized in Table 2 The multiple comparison of surface hardness among dif-139

ferent groups (Table 3) revealed that surface hardness were significantly higher in the Colgate Sensitive 140

Pro-Relief and NovaMinR groups compared with the GC Tooth Mousse group after pH-cycling test as 141

well as acid resistance test (P < 0.05 for all) No significant difference of surface hardness was found 142

between Colgate Sensitive Pro-Relief and NovaMinR during the pH-cycling test and acid resistance test 143

(P = 0.45 and P = 0.83, respectively).

144

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Fig 2 Representative SEM micrographs of specimens after demineralization and remineralization: (a) after demineralization, the enamel showed a typical prismatic structure; (b) remineralization by CPP-ACP; (c) remineralization by Colgate Sensitive Pro-Relief; (d) remineralization by NovaMinR The enamel surface was covered by an irregular deposition layer in all dentifrice groups, the honeycomb-like structures were not evident (Figs 2b, 2c, and 2d) The layer generated by ACC (Fig 2c) and CSP (Fig 2d) seemed to be more thick and uniform than CPP-ACP (Fig 2b).

3.2 Scanning electron microscopy (SEM)

145

Demineralization affected the surface structure of the enamel, showing demineralized regions with 146

a honeycomb-like appearance and a rough surface without a protective layer (Fig 2a) After 15 days 147

of pH-cycling, the enamel surfaces were remineralized and covered by an irregular deposition layer 148

in all dentifrice groups, sealing most of their regularities (Figs 2b, 2c, and 2d) After an acid attack, 149

some depositions were dissolved; and partially porous enamel was evidenced in the GC Tooth Mousse 150

group (Fig 3a) However, a non-homogeneous thin film with precipitated agents remained visible on the 151

enamel surface in the Colgate Sensitive Pro-Relief and NovaMinR groups (Figs 3b and 3c).

152

3.3 Atomic force microscopic observations

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AFM micrographs of the demineralized specimens displayed a significant depression with prismatic 154

structures of HCA and loss of enamel materials from the surfaces (Fig 4a) The surface roughness (Ra) 155

in all groups significantly increased almost three times after demineralization, averagely from 45 ±

156

2 nm to 123 ± 5 nm (P < 0.05 for all) (Table 4) The remineralization treatments by different

den-157

tifrices significantly reduced the Ra values to 125± 2 nm, 112 ± nm, 106 ± 3 nm and 102 ± 3 nm

158

in the control, GC Tooth Mousse, Colgate Sentsitive Pro-Relief and NovaMinR groups, respectively. 159

In addition, surface mineral layers formed by Colgate Sentsitive Pro-Relief (Fig 4c) and NovaMinR 160

(Fig 4d) treatments were relatively uniform and homogeneous After the acid resistance test, the de-161

posited crystals on the enamel surfaces were dissolved at the varying degrees (Fig 5); and the Ra value 162

of GC Tooth Mousse group (152± 5 nm) was significantly higher than Colgate Sensitive Pro-Relief

163

(144± 4) and NovaMin R (145± 5) group No significant difference of Ra was found between Colgate

164

Sensitive Pro-Relief and NovaMinR during the pH-cycling test and acid resistance test (P > 0.05 for 165

both)

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Table 4 Surface roughness (Ra, nm) of enamel at different stages

126± 8b2

112± 6d3

152± 5g4

Colgate Sensitive Pro-Relief 45± 2a1

120± 3b2

106± 3e3

144± 4h4

123± 3b2

102± 3e3

145± 5h4

Same lowercase letter indicated no statistical difference in columns Same number indicated no statistical difference in rows (P < 0.05) DM, demineralization; RM, remineralization; ART, acid resistance testing.

Fig 3 Representative SEM micrographs of specimens after acid resistance test: (a) CPP-ACP; (b) Colgate Sensitive Pro-Relief; (c) NovaMinR The deposited crystals in enamel surfaces were partially dissolved, in CPP-ACP group the Enamel prism and interprism structures became slightly evident (Fig 3a) However, a film with precipitated agents remained visible on the enamel surface in the ACC and CSP groups (Figs 3b, 3c).

4 Discussion

167

The present study demonstrates that Colgate Sensitive Pro-Relief and NovaMinR are superior in pro-168

moting remineralization and inhibiting demineralization over CPP-ACP containing toothpastes These 169

present results were somehow in line with the results of other studies [15,16] Mehta A [15] compared 170

the remineralization efficiency of NovaMinR and CPP-ACP containing dentifrices After remineraliza-171

tion the mean microhardness in NovaMinR group was 371.76 and in CPP-ACP group was 357.07, the 172

difference between the two groups was found to be statistatically significant, indicating NovaMinR den-173

tifrices demonstrated a better remineralization potential than CPP-ACP Elizabeta G and John W [16] 174

observed morphological changes in remineralized enamel surfces by Scanning Electron Microscope, and 175

found that deposits formed by NovaMinR were larger and angular than deposits created by CPP-ACP. 176

The high KNH values for NovaMinR treatments may be due to its firm attachment to the enamel surface 177

by means of a layer that has a composition similar to enamel, unlike the amorphous nature of CPP-ACP 178

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(a) (b) (c) (d)

Fig 4 Representative AFM images of specimens after demineralization and remineralization: (a) after demineralization; (b) treated with CPP-ACP; (c) treated with Colgate Sensitive Pro-Relief; (d) treated with NovaMinR Figure 4a showed the honey-comb-like structures after demineralization The enamel surface was covered with globular mineral particles (Figs 4b, 4c, and 4d) (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/THC-161221)

Petrou et al [17] proposed that the combination of arginine and calcium carbonate favors calcium 179

and phosphate ions to deposit dentin-like minerals within dentin tubules and on the dentin surface This 180

combination works on the principle of organic-inorganic interactions similar to the mineralization of 181

natural tissues (biomimetic approaches) The role of arginine is similar to the organic matrix in the 182

mineralization process [18] Organic molecules (such as arginine) are positively charged on the surface 183

or hidden inside structural folds [17] These organic molecules act as a nucleation center for mineral-184

ization, as a result of strong electrostatic interactions and precipitating inorganic minerals Depositions 185

that contained calcium, phosphate and arginine were revealed after exposure to an acid challenge for 186

two minutes, which was performed to simulate the consumption of an acidic beverage Acid resistance 187

of the deposition ensures the lasting remineralization of toothpastes In the present study, specimens 188

treated with arginine (8%) and calcium carbonate revealed less reduction of surface hardness after the 189

acid resistance test, compared with the specimens in the CPP-ACP and control groups

190

Remineralization occurs when calcium and phosphate ions are redeposited on the effected enamel 191

surface crystals The primary source of calcium and phosphate ions is saliva The low concentration of 192

calcium and phosphateions in saliva limits its remineralization capacity [19] The three different tooth-193

pastes used in the study include calcium phosphate-based systems; and their remineralization capacities 194

were mainly based on the enhancement of the natural remineralization by salivas [20]

195

PH-cycling models have been broadly used in laboratories to evaluate the progress of carious le-196

sions [21] The pH-cycling protocol carried out in the present study was in accordance to the protocol 197

used by Ten Cate and Duijsters [22] In order to simulate the daily routine of oral environment, this model 198

was designed to apply toothpastes three times a day, i.e early morning, midday and before bed-time 199

NovaMinR is a calcium-phosphate based bioactive glass that releases sodium, calcium, phosphorous 200

and silica ions to form HCAdirectlywithout the intermediate ACP phase [15] It has been found that ions 201

were released and transformed to HCA in up to two weeks [12] And the average time for CPP-ACP 202

to remineralize after an acid challenge is also approximately two weeks [23] Considering this fact, the 203

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(a) (b) (c)

Fig 5 Representative AFM images of specimens after acid resistance test: (a) CPP-ACP; (b) Colgate Sensitive Pro-Relief; (c) NovaMinR After an acid attack, some depositions were dissolved, the prismatic structure of hydroxyapatite in ACC (Fig 5b) and CSP (Fig 5c) group were less visible than CPP-ACP group (Fig 5a) (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/THC-161221)

Fig 6 Surface roughens (Ra) of enamel blocks at different stages measured by Atomic force microscopy (AFM) (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/THC-161221)

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current study was designed to carry out pH-cycling for 15 days.

204

Surface hardness testing has been widely used to assess the changes of surface mechanical properties 205

during the demineralization/remineralization process since it is a relatively simple, rapid, noninvasive 206

and reproducible technique [24] The hardness of mineralized hard tissues is directly related to its min-207

eral content Loss of minerals from enamel (for example, in cases of caries or acid etching) affects 208

surface mechanical properties including hardness The microhardness of demineralized specimens was 209

observed to decrease in all groups, but increased after pH-cycling Colgate Sensitive Pro-Relief and 210

NovaMinR exhibited a significantly higher efficacy in enhancing remineralization after pH-cycling. 211

Both the ACC and CSP groups continued to present significantly less microhardness loss compared to 212

the other groups

213

Both SEM and AFM were used in the study to evaluate the changes of enamel surface morphol-214

ogy and roughness at different stages AFM has been reported offered relatively better resolution and 215

high-contrast images than SEM [25] Furthermore, AFM can display a more intuitive three-dimensional 216

picture of the outermost layer of the enamel surface, even at a nanometer scale The characterization 217

of SEM and AFM for dentifrice-treated specimens revealed that enamel surfaces were covered by a 218

superficial layer of precipitated crystals to repair the erosive enamel, suggesting the remineralizing abil-219

ity of these three treatments These findings were consistent with microhardness test results After the 220

acid resistance test, SEM and AFM images revealed that partial depositions were dissolved, and that 221

some cavities were covered by a protective layer before the test, which was observed in the CPP-ACP 222

group (Fig 3a) Enamel prism and interprism structures became slightly evident (Fig 5a) A homoge-223

neous layer covering the erosive enamel surfaces was observed in the Colgate Sensitive Pro-Relief and 224

NovaMinR groups, which was supported by results of the surface hardness tests.

225

This study demonstrates a promising potential of topical agents for remineralization of early enamel 226

caries lesions Further researches, especially in vivo studies, are still needed to provide quality evidences

227

for clinicians to treat early enamel caries lesions in a relatively non-invasive way to conserve tooth 228

structure and underlying pulp tissues

229

5 Conclusion

230

Despite the limitations of in vitro studies, all tested bioactive toothpastes were found to be effective in

231

enhancing remineralization, Colgate Sensitive Pro-Relief and NovaMinR present a significant advantage 232

in promoting remineralization and inhibiting the demineralization of early enamel carious lesions in 233

comparison with GC Tooth Mousse

234

Acknowledgement

235

This study was supported by the grants from the Key Project supported by Medical Science and 236

Technology Development Foundation, Nanjing Department of Health (No YKK14111)

237

References

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[1] Lynch E, Baysan A Reversal of primary root caries using a dentifrice with a high fluoride content Caries Res 2001; 35:

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60-64.

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[2] Backer Dirks O Posteruptive changes in dental enamel J Dent Res 1966; 45: 503-511.

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