ORIGINAL ARTICLE

Surface deterioration and elemental composition of retrieved orthodontic miniscrews Pradnya Patil,a Om Prakash Kharbanda,b Ritu Duggal,c Taposh K. Das,d and Dinesh Kalyanasundarame New Delhi, India

Introduction: This study provides insight into surface and elemental analyses of orthodontic retrieved miniscrew implants (MSIs). The sole purpose was to investigate the behavior of MSIs while they are in contact with bone and soft tissues, fluids, and food in the oral cavity. The information thus gathered may help to understand the underlying process of success or failure of MSIs and can be helpful in improving their material composition and design. Methods: The study was carried out on 28 titanium-alloy MSIs (all from the same manufacturer) split into 3 groups: 18 MSIs were retrieved after successful orthodontic treatment, 5 were failed MSIs, and 5 were as-received MSIs serving as the controls. All MSIs were subjected to energy dispersive x-ray microanalysis to investigate the changes in surface elemental composition and to scanning electron microscopy to analyze their surface topography. Data thus obtained were subjected to suitable statistical analyses. Results: Scanning electron microscope analysis showed surface manufacturing imperfections of the as-received MSIs in the form of stripes. Their elemental composition was confirmed to the specifications of the American Society for Testing of Materials for surgical implants. Retrieved MSIs exhibited generalized surface dullness; variable corrosion; craters in the head, neck, body, and tip regions; and blunting on tips and threads. Energy dispersive x-ray analyses showed deposition of additional elements: calcium had greater significance in its proportion in the body region by 0.056 weight percent; iron was seen in greater proportion in the failed retrieved MSIs compared with the successful miniscrews; cerium was seen in greater proportions in the head region by 0.128 weight percent and in the neck region by 0.147 weight percent than in the body and tip regions of retrieved MSIs. Conclusions: Retrieved MSIs showed considerable surface and structural alterations such as dullness, corrosion, and blunting of threads and tips. Their surfaces showed interactions and adsorption of several elements, such as calcium, at the body region. A high content of iron was found on the failed MSIs, and cerium was seen in the head and neck regions of retrieved MSIs. (Am J Orthod Dentofacial Orthop 2015;147:S88-100)

a

Postgraduate student, Division of Orthodontics and Dentofacial Deformities, Centre for Dental Education and Research, All India Institute of Medical Sciences, New Delhi, India. b Professor and head, Division of Orthodontics and Dentofacial Deformities, Centre for Dental Education and Research, All India Institute of Medical Sciences, New Delhi, India. c Professor, Division of Orthodontics and Dentofacial Deformities, Centre for Dental Education and Research, All India Institute of Medical Sciences, New Delhi, India. d Additional professor, Department of Anatomy; officer in charge, Electron Microscope Facility, All India Institute of Medical Sciences, New Delhi, India. e Assistant professor, Centre for Biomedical Engineering, Indian Institute of Technology, Delhi; assistant professor, Department of Biomedical Engineering, All India Institute of Medical Sciences, New Delhi, India. All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and none were reported. Address correspondence to: Om Prakash Kharbanda, Division of Orthodontics and Dentofacial Deformities, Centre for Dental Education and Research, All India Institute of Medical Sciences, New Delhi 110029, India; e-mail, opk15@hotmail. com. Submitted, July 2014; revised and accepted, October 2014. 0889-5406/$36.00 Copyright Ó 2015 by the American Association of Orthodontists. http://dx.doi.org/10.1016/j.ajodo.2014.10.034

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he orthodontic miniscrew, a temporary anchorage device, was introduced by Gainsforth and Higley1 in an animal study. In each of 5 dogs, a Vitallium screw was placed in the anterior border of the ramus of the mandible to apply traction by means of an orthodontic elastic connected to a maxillary appliance for skeletal anchorage. However, Kanomi2 in 1997 first described the “mini-implant” specifically designed for orthodontic applications. Over the last 2 decades, titanium miniscrews have gained enormous popularity in orthodontics and are often regarded as the source of absolute intraoral anchorage for clinical purposes.3 The popularity of these devices is due to their low cost, small dimensions, ease of insertion and removal, and the possibility of applying immediate loading, thereby reducing the total orthodontic treatment duration.4,5 The introduction of miniscrew implants (MSIs) in the orthodontic armamentarium has widened the scope and envelope of orthodontic treatment to some extent. It is possible

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to treat patients with moderate to severe skeletal discrepancies and obtain complex tooth movements that were not possible previously. Compared with other forms of compliance-dependent anchorage, MSIsupported anchorage offers a more predictable outcome. MSIs are manufactured from commercially pure titanium and grade V titanium alloy. Titanium alloy is favored because of its higher strength relative to commercially pure titanium. Contemporary MSIs are designed for ease of insertion and are generally safe to use. However, they have been reported to cause gingival injuries and have occasionally been found to undergo fracture because of mechanical failure in the oral environment. Failed MSIs necessitate their removal or replacement.6 Several factors influence the success of orthodontic MSIs, including careful patient selection, the characteristics of the implantation site, and the macrostructure and microstructure properties of the implants.7-9 Even though titanium alloys are known to be exceptionally corrosion resistant because of the stability of the passive titanium oxide layer on the surface, MSIs have been reported to undergo corrosion after clinical applications.10 Generally, corrosion is observed when the titanium oxide film breaks down locally, and rapid dissolution of the underlying metal occurs in the form of pits.11 Crevice corrosion occurs between 2 close surfaces or in constricted places where oxygen exchange is not available.11 When an implant is milled and placed in bone, the stress on the MSI might lead to stress corrosion or cracking of the alloy. This cracking may propagate in the physiologic or the corrosive environment. Once the required orthodontic objectives have been achieved, the MSIs are removed from patient's bone. After removal, the retrieved devices are usually discarded. However, economic factors or environmental conservation might influence clinicians to consider reusing MSIs. Not all temporary implant devices can be reused, but metal implants, such as those made from titanium alloy, may be more amenable to reuse because they can be mechanically and chemically cleaned and resterilized with potentially little or no loss of form or function.12 Several studies related to mechanical, chemical, and surface characteristics of prosthetic dental implants are available in the literature.13-15 On the other hand, we located 4 studies describing the surface and mechanical natures of retrieved orthodontic MSIs.8,16-18 Eliades et al8 characterized the morphologic, structural, and compositional alterations, and assessed the changes in the hardness of orthodontic MSIs retrieved after successful service. They reported that used titanium-alloy MSIs have morphologic and surface structural alterations.

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Their Vickers microhardness testing showed no change in surface hardness of the retrieved specimens compared with the controls. Mattos et al16 compared the surface morphology and fracture torque resistance of as-received, sterilized, and retrieved mini-implants to evaluate the fracture risks of reusing orthodontic miniimplants after sterilization. They reported that no defects or corrosion could be identified in autoclaved and retrieved mini-implants, but worn surfaces and scratch marks were observed. A statistically significant difference in the fracture torque was observed between the as-received and retrieved groups. Sebbar et al17,18 assessed the surface changes in MSIs retrieved after usage and compared them with as-received MSIs under an optical microscope. Used MSIs showed signs of corrosion mainly at the sites of manufacturing defects. The literature lacks comprehensive information on used miniscrews regarding their surface and elemental composition. Therefore, a study aimed at surface and elemental analyses of successful miniscrews after retrieval compared with failed and as-received miniscrews was undertaken. Our sole purpose was to investigate the behavior of MSIs while in contact with bone and soft tissues, oral fluids, and food. The information thus gathered may help orthodontists to understand the intricacies of success or failure of MSIs related to their design and material composition. MATERIAL AND METHODS

This study was conducted with 28 MSIs, 8 mm long, 1.5 mm in diameter, bracket head type, self-drilling, made from grade V titanium alloy. All MSIs were procured from same manufacturer (Absoanchor; Dentos, Daegu, Korea) to prevent any bias in design and material properties. Of the 28 MSIs, 18 were retrieved from patients after successful service of 12.89 6 5.33 months. Five MSIs, which had to be retrieved because of loosening failure during treatment (duration, 6.8 6 2.86 months), constituted the failed retrieved group. All MSIs were retrieved from buccal interradicular bone between the second premolar and the permanent first molar. These retrieved MSIs were used in 8 patients (4 male, 4 female; mean age, 17.75 6 6.08 years) with Class I bimaxillary protrusion malocclusions. These MSIs were used for en-masse retraction of anterior teeth (11 in the maxillary arch, 12 in the mandibular arch). An orthodontic force of 200 g was applied on each MSI. We used Nitinol closed-coil springs of 9 mm length (GAC International Inc, Central Islip, NY), which applied a consistent retraction force. These retrieved miniscrews were part of the ongoing research in which a standard protocol of insertion and force application was used.

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Table I. Physical properties of maxillary bone, artifi-

cial bone model, and MSI Material Cortical bone in maxillary region Cancellous bone in maxillary region Artificial bone model outermost layer representing cortical bone (made with short fiber-filled epoxy sheets) Artificial bone model core layer representing cancellous bone (made with solid polyurethane foam) MSI

Fig 1. Four zones of investigation on the surface of an MSI.

Informed consent was obtained from all patients before MSI placement. Five as-received MSIs served as the control group. Each MSI was retrieved with a long-hand driver supplied by the manufacturer, consisting of body and tip. After removal, each MSI was gently washed and stored completely immersed in fresh deionized water in an autoclaved glass vial duly labeled.12,16 Deionized water was considered a suitable medium for storage because it has been reported to be free from any other elements and has the least effect on the dissolution of elements from the cementum of premolars. In addition to its inertness, it also has minimal effects on physical properties such as the hardness and the elastic modulus of teeth.19 Analyses by energy dispersive x-ray microanalysis (EDX) and scanning electron microscopy (SEM) were done at 4 zones of each MSI: head, neck, body, and tip (Fig 1). These zones were considered unique because each zone is exposed to a different environment in the body. The head is exposed to oral fluids and food, whereas the neck is in contact with oral mucosa and gingiva, and the body is in contact with bone. Although the tip is immersed in bone, it may show a difference in behavior compared with the body because of its tiny dimensions. Cortical and cancellous bone properties are given in Table I. Each MSI was mounted on a carbon stub and kept in a dessicator for 24 hours. An EDX detector (Oxford Instruments, Abingdon, Oxfordshire, United Kingdom) was used to investigate their elemental composition with an x-ray microanalysis detector. The quantitative analysis of the percentage of weight concentration of the probed elements was performed with an INCA microanalyzer (version 4.06; Oxford Instruments). The carbon quantification was excluded from this study because of

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Elastic modulus (GPa) 14.7 1.5 16.7

Density (kg/m3) 2000 1000 1660

0.759

0640

96

4620

the technical limitation of the EDX in an electron microscope.20 Elements with lower atomic masses such as carbon (atomic number 6 and lower) are difficult to distinguish from each other using EDX. The carbon x-rays have low energy and are easily absorbed by the x-ray detector windows. Furthermore, there can be a significant carbon background signal because of hydrocarbon contamination. Hydrocarbons from the chamber surfaces, vacuum pumps, and sample surface migrate and react with the electron beam to form a black spot that is rich in carbon.20 After elemental analysis with the EDX, the retrieved MSIs were subjected to a cleaning cycle of 30 minutes in an ultrasonicator, completely immersed in enzymatic detergent (Cidezyme; ASP: a Johnson and Johnson company, Irvine, Calif) so that organic debris would be removed and the surface topography of the MSIs could be fully observed under the microscope.16 After cleaning, they were again mounted on carbon stubs and kept in a dessicator for 24 hours, and surface images were taken with SEM (Leo 435VP; SEMTech Solutions, Cambridge, United Kingdom). Alterations of surface changes were looked for: eg, crevice corrosion, corrosion surface damages, dullness, cracks, craters, fractures, and blunting (Table II). After initial scanning of each zone, images of the damaged features or areas were captured. Multiple images of each zone of the MSI were taken; the number of images varied for each zone (about 2-4 images per zone of each MSI). Digital images were obtained at various magnifications (20-500 times) in an incremental manner. Experimental conditions were vacuum at 10 4 mm of mercury; extra high tension voltage level, 20 keV; working distance, 37 mm; and dead time, below 30%. Statistical analysis

The statistical analysis of the data was performed using SPSS statistical software (version 20; IBM, Armonk, NY). The Kruskal-Wallis and the Wilcoxon rank sum tests

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Table II. Surface changes on MSIs and comparisons between 3 groups and 4 zones: values depict the number of sites on which the surface changes were present Corrosion surface damage Zone/Group Head C FR SR Neck C FR SR Body C FR SR Tip C FR SR

S

T

0 7 31

15 15 54

0 7 28

Dullness P value

S

T

0.49

0 5 18

5 5 18

15 15 54

0.72

0 5 18

0 12 54

15 15 54

0.009*

0 7 47

15 15 54

0.001*

Cracks P value

S

T

0*

0 0 5

5 5 18

5 5 18

0*

0 0 0

0 5 18

5 5 18

0*

0 5 18

5 5 18

0*

Craters P value

S

T

0.4

0 1 4

5 5 18

5 5 18

NA

0 3 8

0 0 3

5 5 18

1

0 1 3

5 5 18

1

Fracture P value

Blunting P value

S

T

P value

S

T

0.79

0 0 2

5 5 18

1

5 5 18

0.14

0 0 0

5 5 18

NA

0 3 18

5 5 18

0*

0 0 4

5 5 18

0.41

0 5 18

5 5 18

0*

0 1 7

5 5 18

0.35

0 0 2

5 5 18

1

0 5 18

5 5 18

0*

NA

NA

S, Number of sites in each zone where the parameter was present; T, total number of sites examined in each zone; NA, not applicable; C, control MSIs; FR, failed MSIs; SR, successful MSIs. *P \0.05 was statistically significant; Fischer exact test applied.

were applied to compare the EDX data on elemental composition, and the chi-square test was used for the comparison of the SEM results. We had 3 groups (control, and successful and failed MSIs) and 4 zones (head, neck, body, and tip). To understand the variations, 2 types of analysis were performed: comparisons among the groups and zones, and multiple comparisons between any 2 groups at a time. The Kruskal-Wallis method was used to find the P values among the 3 groups; P values less than 0.05 were considered significant. In the case of multiple comparisons within the 3 groups—analyzing any 2 groups at a time—post hoc analysis of variance was done with the Wilcoxon rank sum method and the Bonferroni correction; P values less than 0.016 were considered significant. The Kruskal-Wallis and Wilcoxon rank sum test results are shown in Tables III and IV. To understand the effects of frictional resistance encountered during miniscrew insertion and removal in bone, an experiment was simulated using artificial bone model (Sawbones; Pacific Research Laboratories, Vashon Island, Wash). The artificial bone block has short fiber-filled epoxy sheets (1 mm) and solid rigid polyurethane foam (40 per cubic foot) representing cortical and cancellous bones, respectively (Table I).21 Five asreceived MSIs with similar specifications were used. Each MSI was inserted into the artificial bone at an angle of 45 with a screwdriver in an artificial bone model block of 2 3 2 in mounted on a fixer. The MSI was immediately

removed by unscrewing it with the same screwdriver. The technique of insertion and removal simulated the method used in the clinical environment. Each MSI was packed in an airtight bag and observed by SEM according to the protocol described above. The artificial bone experiment was done after our study as an additional subset experiment to corroborate our findings: ie, to analyze whether bone friction alone could have caused the kind of surface damage seen in the retrieved MSIs. This subset was not used for data analysis with the above-mentioned 3 groups for evaluation. RESULTS

The as-received MSIs (control) showed a relatively smooth appearance to the naked eye but had surface milling and polishing defects (manufacturing defects) in the form of stripes and scratches (Figs 2, A, and 3, A and C). Dullness was present in retrieved MSIs (successful and failed) at all the sites. In the retrieved MSIs from the artificial bone model, minimal blunting at the tip and dullness was seen compared with the asreceived group; however, no other findings such as corrosion or surface damage were evident. Crevice corrosion, which occurs in the crevices between the implant and the tissue, was prominent on the retrieved MSIs. Other forms of corrosion such as pitting and fretting would be difficult to distinguish without elaborate experiments. Hence, for this study,

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Table III. EDX findings on surface elements (weight percent) of control (C), failed retrieved (FR), and successful

retrieved (SR) MSIs: single comparison (Kruskal-Wallis test)

Element/Group Titanium C FR SR Aluminum C FR SR Vanadium C FR SR Oxygen C FR SR Calcium C FR SR Iron C FR SR Cerium C FR SR Nitrogen C FR SR

P value for comparison within groups

P value for comparison within zones

Head

Neck

Body

Tip

89.75 6 0.07 73.264 6 14.084 84.395 6 5.489

89.75 6 0.07 75.202 6 13.848 74.222 6 14.408

89.75 6 0.07 82.018 6 9.728 90.322 6 1.641

89.75 6 0.07 73.295 6 16.854 70.871 6 14.16

0.03*

0.67

5.97 6 0.01 3.762 6 1.536 4.304 6 2.739

5.97 6 0.01 2.755 6 2.055 2.769 6 2.341

5.97 6 0.01 3.659 6 2.926 0.805 6 0.300

5.97 6 0.01 2.92 6 1.568 2.534 6 1.421

0.001*

0.656

4.07 6 0.07 3.276 6 2.248 0.811 6 1.404

4.07 6 0.07 1.69 6 1.477 0.865 6 1.499

4.07 6 0.07 1.786 6 1.581 2.071 6 3.558

4.07 6 0.07 1.502 6 1.349 1.249 6 1.093

0.001*

0.639

0.10 6 0.01 11.354 6 18.002 8.795 6 4.008

0.10 6 0.01 19.011 6 9.385 21.302 6 11.253

0.10 6 0.01 10.186 6 8.183 5.813 6 5.105

0.10 6 0.01 19.985 6 12.829 23.742 6 11.344

0.009*

0.384

0.00 6 0.00 0.215 6 0.187 0.162 6 0.169

0.00 6 0.00 0.17 6 0.03 0.15 6 0.026

0.00 6 0.00 0.165 6 0.181 0.221 6 0.229

0.00 6 0.00 0.189 6 0.17 0.139 6 0.144

0.031*

0.529

0.00 6 0.00 0.504 6 0.161 0.305 6 0.329

0.00 6 0.00 0.87 6 0.116 0.59 6 0.102

0.00 6 0.00 0.387 6 0.374 0.160 6 0.204

0.00 6 0.00 0.266 6 0.076 0.114 6 0.129

0.045*

0.218

0.00 6 0.00 0.126 6 0.149 0.131 6 0.228

0.00 6 0.00 0.184 6 0.318 0.111 6 0.097

0.00 6 0.00 0.00 6 0.00 0.00 6 0.00

0.00 6 0.00 0.00 6 0.00 0.00 6 0.00

0.136

0.049*

0.00 6 0.00 2.58 6 3.62 1.97 6 3.90

0.00 6 0.00 3.04 6 4.58 1.70 6 2.62

0.00 6 0.00 1.54 6 1.45 5.86 6 11.61

0.00 6 0.00 0.00 6 0.00 0.02 6 0.06

0.293

0.412

*P \0.05 was statistically significant.

we called all such changes “corrosion surface damage.” Corrosion surface damage and craters were greater in the retrieved MSIs (greater in the successful retrieved group than in the failed retrieved group); there were none in the control group. Corrosion surface damage was greater at the body and tip regions (Figs 2, B, and 3, B). Craters were most common at the body region and least common at the head region. No significant cracks and fractures were evident in the control group but were seen on 4 retrieved MSIs (Fig 2, C and D). Blunting was present in all retrieved MSIs at the tips and threads and was absent in the controls (Fig 3, C and D) (Table II). In the immediately retrieved MSIs from the artificial bone model, no other findings such as corrosion or other surface damage were evident; however, minimal blunting at the tip and dullness were seen compared with the as-received group.

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The surface elemental composition of as-received MSIs was found to be within the ASTM standard (F136-13). Retrieved MSIs showed adsorption of oxygen, nitrogen, calcium, phosphorus, iron, fluorine, sodium, chlorine, magnesium, cerium, and potassium in varying amounts (Table III; Fig 4, A and B). Statistically significant findings were as follows. Calcium was in greater proportion in the successful retrieved group than in the failed retrieved group in the body region by 0.056 weight percent (P 5 0.0149) (Fig 5, A) (Tables III and IV). Iron was in greater proportion at all 4 zones in the failed MSIs than in the successful MSIs (P 5 0.045) (Tables III and IV) by 0.199 weight percent in the head region, by 0.28 weight percent in the neck region, by 0.227 weight percent in the body region, and by 0.152 weight percent in the tip region (Fig 5, B). Cerium was in greater proportion in the

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Table IV. EDX findings on surface elements (weight

percent) of control (C), failed retrieved (FR), and successful retrieved (SR) MSIs: multiple comparisons within groups (Wilcoxon rank sum test): numbers depict P values of comparisons Zone/Element Head Ti Al V O Ca Fe Ce N Neck Ti Al V O Ca Fe Ce N Body Ti Al V O Ca Fe Ce N Tip Ti Al V O Ca Fe Ce N

C (n 5 5) vs FR (n 5 5)

FR (n 5 5) vs SR (n 5 18)

SR (n 5 18) vs C (n 5 5)

0.0086* 0.0086* 0.0086* 0.0086* 0.0411 0.0647 0.0539 0.0521

0.4561 0.5023 0.4123 0.6018 0.0568 0.0121* 0.3653 0.7815

0.0008* 0.0008* 0.0008* 0.0008* 0.0568 0.0324 0.1094 0.0527

0.0086* 0.0086* 0.0273 0.0086* 0.0973 0.0860 0.0539 0.0451

0.4123 0.4123 0.4123 0.136 0.9178 0.0098* 0.3923 0.3615

0.0008* 0.0008* 0.0022* 0.0008* 0.2594 0.0457 0.0396 0.0578

0.0086* 0.115 0.115 0.0086* 0.0489 0.0539 NA 0.0524

0.2051 0.8815 0.8815 0.1547 0.0179 0.0111* NA 0.0203

0.0017* 0.0017* 0.0112* 0.1339 0.0079* 0.1478 NA 0.0186

0.0459 0.0459 0.115 0.115 0.0317 0.0539 NA 0.1547

0.8231 0.8231 0.8815 0.1563 0.0187 0.0132* NA 0.8812

0.0017* 0.0017* 0.0029* 0.009* 0.0014* 0.446 NA 0.8812

NA, Not applicable: indicates that both sets of data points had only a numeric value of zero; hence, no comparison could be made. Ti, Titanium; Al, aluminum; V, vanadium; O, oxygen; Ca, calcium; Fe, iron; Ce, cerium; N, nitrogen. *P \0.016 was statistically significant.

head region by 0.128 weight percent and the neck region by 0.147 weight percent than in the body and tip regions of the retrieved MSIs (P 5 0.049), and there was none in the control group (Tables III and IV; Fig 5, C). No significant difference was found in the MSIs retrieved from the maxilla and the mandible in the SEM and EDX investigations. In this study, no prior sample size calculation could be done at the planning stage because of the nature of

the experiment and the scarce information available. At the end of the study, the power calculation was computed separately for surface changes (SEM) and EDX data based on the results. For the surface-change (SEM) data, the surface alterations of all 4 zones of each MSI (head, neck, body, and tip) were summed as the number of alterations per MSI. Subsequently, means and standard deviations of surface changes were derived and computed for each group separately: control, failed retrieved, and successful retrieved. The power values of the study (at the 95% confidence level and 5% alpha) were control vs failed retrieved, 100%; control vs successful retrieved, 100%; and successful retrieved vs failed retrieved, 91%. For the EDX data, we used calcium and cerium as representative denominators because these exhibited major variations. Quantitative values of calcium for the body and tip regions and of cerium for the head and neck regions were used. The computed power values to detect mean differences of calcium in the tip region between control vs failed retrieved, control vs successful retrieved, and failed retrieved vs successful retrieved were 14%, 82%, and 61%, respectively. For the same groups in the body region, the power values were 58%, 60%, and 60%, respectively. The power for cerium was weak. In the control vs failed retrieved, control vs successful retrieved, and failed retrieved vs successful retrieved, the power values were 38%, 30%, and 18% for the neck region and 26%, 23%, and 10% for the head region, respectively. DISCUSSION

Retrieval analysis is an emerging field in biomedical materials because of the critical information it provides on the performance of the material in the environment in which it is intended to function. The development of international standards for the retrieval analysis of biomaterials strongly indicates the significance of this method in studying the performance of materials.22,23 Our results indicate substantial changes in the surface profiles of MSIs and the presence of impurities precipitated on the surfaces of retrieved MSIs, which are attributed to contact of the implant with oral tissues, biologic fluids, blood and exudates, saliva, and food.8 Retrieved MSIs showed loss of gloss and surface finish, resulting in a dull surface at all 4 examined zones.8 It was assumed that insertion and removal of miniscrew causes the surface to wear out to some extent. Blunting of threads and tip (less sharp thread and tip compared with as-received screws)16 was also linked to wear during the process of insertion and removal (Fig 3, D), and so

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Fig 2. A, Threaded body region of as-received MSI at 500-times magnification (arrow) (micromarker, 200 mm); B, wear type of corrosion defect on thread of retrieved MSI at 500-times magnification (arrow) (micromarker, 200 mm); C, crack on thread of retrieved MSI at 500-times magnification (arrow) (micromarker, 200 mm); D, fracture on a thread of retrieved MSI at 500-times magnification (arrow) (micromarker, 200 mm).

the occasional fracture of the thin thread at its outermost border or tip was attributed to poor mechanical strength in these regions (Fig 2, C and D). A subset of 5 miniscrews used in a simulated experiment on artificial bone showed only minor blunting of the tips and dullness of the surfaces of the screws. Therefore, it appears that in addition to physical bone contact during insertion and removal, other factors may have also contributed to the major surface changes on the MSIs, and these will be elaborated in the ensuing paragraphs. If the implant pierces the mucosa and drills in bone, it causes traumatic inflammation, including reduction of the pH in the early exudative phases, activation of cells including polymorphonuclear granulocytes and macrophages, and release of proteins, enzymes, and oxidizing agents that might contribute to the surface alterations.8 A primary requisite for any metal used in the mouth is that it must be biocompatible and should not corrode when in contact with the tissues. Factors such as temperature, quantity and quality of saliva, plaque, pH, proteins, the physical and chemical properties of foods and liquids, and oral health conditions can influence corrosion.9 The composition of saliva varies considerably

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between persons and at different times. Saliva, a physiologic fluid in oral cavity, also has variations in pH at different times of the day and among different persons (pH 5 6.2-7.4).24 Moreover, oral hygiene has a strong effect on the corrosiveness of the oral environment. Titanium alloys used to manufacture MSIs are less resistant to corrosion because the alloys represent discontinuities in the protective oxide film.11 The surface milling and polishing defects during the manufacturing process are seen in the form of stripes and scratches. These tiny defects can be a starting point for electrochemical attack when miniscrews are inserted in the body.17 Although titanium alloys are considered highly corrosion resistant because of the stable passive titanium oxide layer on the surface, they are not inert to corrosive attack. When the stable surface oxide layer breaks down or is removed and cannot reform on parts of the surface, titanium can be corrosive, as are many other base metals.25 Titanium has a high coefficient of friction. Corrosion takes place when the passive oxide film is worn off from contact with bone. Wear particles may form because of corrosion (Fig 2, B).11 This type of corrosion is responsible for most of the metal released

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Fig 3. A, Junction between the body and thread regions of as-received MSI at 70-times magnification (arrow) (micromarker, 1 mm); B, crevice corrosion at the junction between the body and thread regions of MSI at 70-times magnification (arrow) (micromarker, 1 mm); C, tip of as-received MSI at 500-times magnification (arrow shows the tip region; circle shows the smooth surface) (micromarker, 200 mm); D, blunting of the tip of retrieved MSI at 500-times magnification (arrow shows the blunt tip region; circle shows the deposition) (micromarker, 200 mm).

into tissues.26-28 In contrast, pure titanium is highly resistant to corrosion in any in-vivo environment likely to be encountered; however, its low strength limits its use as an implant. The mechanical load on orthodontic MSIs is nonvibrating and nondynamic. Also, because the bone is softer than the implant, the damaging effects on the implant surfaces from mechanical loading are assumed to be minimal. Therefore, the surface damage on the oxide layer during insertion can be significant in contributing to corrosion.29 Crevice corrosion (Fig 3, B) occurs between 2 close surfaces or in constricted places, trapping a stagnant layer of solution where oxygen exchange is not available. This is because pH in the crevices can be as low as 2 (highly acidic) for a 7 pH (neutral) solution.30 The reduction in pH further causes initiation and propagation of the crevice corrosion phenomenon. When the acidity of the milieu increases with time, the passive layer of the alloy dissolves, and it accelerates the local corrosion process. Natural convection no

longer allows the trapped solution to mix with the bulk solution outside, so that diffusion is the only form of mass transport by which dissolved oxygen can enter the occluded region. In such crevices, the supply of dissolved oxygen in the trapped solution can be depleted. As a result, the anodic corrosion reaction occurs in the crevices, and the supporting cathodic reduction reaction occurs on the much larger surfaces outside the crevices.30 Crevice-like geometric patterns were observed on threads, tips, heads, and junctions of the head-neck and neck-thread regions. This phenomenon explains why more crevice corrosion occurred in these areas of the retrieved miniscrews. A crater is a cavity or hole in any surface.31 A crack is a line on the surface of something along which it has split without breaking apart.32 A fracture is the cracking or breaking of a hard object or material.13 In our study, corrosion surface damage and craters were found to be significantly present in successful retrieved MSIs because the extended periods of retention (12.89 6 5.33 months)

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Fig 4. A, Representative graph of EDX plot of as-received MSI (elemental composition confirmed to ASTM standards); B, representative graph of EDX plot of retrieved MSI (the additional significant elements are oxygen, calcium, iron, and cerium). Ti, Titanium; V, vanadium; O, oxygen; Al, aluminum; N, nitrogen; Mg, magnesium; Ce, cerium; Na, sodium; Fe, iron; P, phosphorus; Ca, calcium; keV, kiloelectronvolt.

in the jaws allowed longer contact with oral tissues and biologic fluids. Surface alterations were seen more frequently in the body region because of the increased surface contact area of the threads. Cracks and fractures were seen mostly in the thread and tip regions. This can be attributed to the decreased thickness of material at these regions. Orthodontic devices in the mouth are subjected to electrochemical corrosion, which leads to gradual surface biodegradation of the surface material by a process of oxidation, and they trigger the release of potentially toxic or allergenic substances.10 Corrosion can severely limit the fatigue life and ultimate strength of the material, leading to mechanical failure of the implants.33,34 Corrosion can lead to roughening of the surface,

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weakening of the implant, liberation of elements from the metal or alloy, and toxic reactions. The liberation of alloy elements and corrosion products can produce discoloration of adjacent soft tissues and allergic reactions such as oral edema, perioral stomatitis, gingivitis, and extraoral manifestation such as eczematous rashes in susceptible patients. Corrosion products have been implicated in causing local pain or swelling near implants in the absence of infection, and they may be carcinogenic.33 Kasemo35 demonstrated the dissolution of corrosion products into the bioliquid and adjacent tissues. The pathomechanism of the impaired wound healing is modulated by specific metal ions,36 and corrosion products released during corrosion influence the function of the participating cell types—eg,

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Fig 5. Graphs of the relative weight percentages of elements on EDX: A, calcium was in greater proportion in the successful retrieved group than in the failed retrieved group in the body region by 0.056 weight percent; B, iron on the surface of the failed MSIs compared with the successful MSIs had higher adsorption rates at all 4 zones (head region, 0.199 weight percent; neck region, 0.28 weight percent; body region, 0.227 weight percent; tip region, 0.152 weight percent); C, cerium was in greater proportion on the head and neck regions of retrieved MSIs (head region, 0.128 weight percent; neck region, 0.147 weight percent). C, Control; FR, failed retrieved; SR, successful retrieved. *P \0.05 was statistically significant.

endothelial cells. Olmedo et al34 reported that macrophages in peri-implant soft tissues induced by a corrosion process play an important role in implant failure. The corrosion products that are released are phagocytosed by macrophages, stimulating the release of inflammatory mediators such as cytokines toward the bone surface, contributing to its resorption by osteoclast activation, and the metallic particles that result from corrosion may directly inhibit osteoblast function, leading to local osteolysis and loss of clinical stability of the MSI.34 The frictional forces during insertion and removal of MSIs alone do not contribute to major surface alterations in the absence of interactions with body fluids and tissues. Corrosion surface damage seen on titanium alloy MSIs is the result of complex interactions

and a time-consuming phenomenon. Therefore, corrosion effects were not seen in the immediately retrieved MSIs in a simulated experiment on artificial bone. For the EDX analysis, the as-received MSIs conformed to the ASTM standards for surgical implants. Titanium, aluminum, and vanadium are the parent elements of grade V titanium alloy, the presence of which was masked because of other elements deposited on the surface of retrieved MSIs: oxygen, nitrogen, calcium, phosphorus, iron, fluorine, sodium, chlorine, magnesium, cerium, and potassium (Fig 4). Since EDX provides data in weight percentages of elements, the 3 parent elements were masked in the retrieved MSIs because of adsorption of other elements over the surface from the local biologic milieu. Oxygen was present relatively in greater proportions in the retrieved MSIs than in the control MSIs

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(Table III); this may have its source from contact with tissues or exposure to the external environment while the MSIs were transported from the autoclaved packet to the bone until insertion and removal.12 It is known that the titanium oxide passive layer is formed on the surface because of contact with oxygen.8 Calcium phosphate precipitates on the titanium oxide layer, changing the outer oxide layer to complex titanium and calcium phosphates. The calcium is derived mainly from the contact of the implant surface with blood involving mainly adsorption of proteinaceous integuments, which are calcified later with the precipitation of calcium and phosphorus.37 Also, bone particles, seen adhering to the miniscrew implant, were derived through intimate contact with alveolar bone.8,38 Calcium was seen in greater proportions in the successful retrieved group than in failed retrieved group in the body region by 0.056 weight percent. Its presence in the successful retrieved MSIs was enhanced by the extended period of retention in alveolar bone of 12.89 6 5.33 months (Fig 5, A).8 X-ray photoelectron spectroscopy characterization study on titanium has shown the presence of titanium 21, titanium 31, and titanium 41 on its surface.39 In other words, the surface oxide film on titanium is not stoichiometric and still has scope for further oxidation. Calcium phosphate was formed when titanium was immersed in Hanks solution. Calcium and phosphate cannot exist stably alone on titanium and eventually formed calcium phosphate on it. The surface oxide film on titanium is thus not completely oxidized and is relatively reactive.39 The greater proportion of iron in the failed MSIs compared with the successful MSIs by 0.214 weight percent (Fig 5, B) was attributed to contact with blood.8 Since peri-implantitis accounts for about 30% of miniscrew failures, we hypothesized that iron comes from the increased blood flow caused by inflammation.40 There were soft tissues covering or in contact with the head and neck of MSIs, but the body and tip regions were in contact with bone, with no soft-tissue contact. Also, there was more iron in the failed MSIs than in the successful ones at the body and tip regions; this suggests that apart from peri-implantitis, bonerelated changes also contribute to MSI failures. The presence of nitrogen on the surface implies proteins that were adsorbed from body fluids.8 More nitrogen was found in the body region of the retrieved MSIs because of the greater surface contact area. Retrieved MSIs exhibited cerium in greater proportions in the head and neck regions by 0.137 weight percent than in the body and tip regions (Fig 5, C). Cerium is a component of a few mouthwashes for its

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antimicrobial properties. Cerium is also present in some foods, such as tubers grown in cerium-rich soils and water.41,42 We attributed mouthwashes and foods as the sources of the cerium on the heads and necks of the retrieved MSIs in our study. Cerium chloride and its combination with fluoride can significantly reduce various mineral losses and the progression of the depth of enamel lesions.41 It is also said to have a bacteriostatic effect.43 A strong binding of cerium nanoparticles to the outer membrane of Staphylococcus aureus causes the inhibition of active transport, dehydrogenase and periplasmic enzyme activity, and thus eventually the inhibition of RNA, DNA, and protein synthesis leading to cell lysis.43 A cerium coating could lead to reduction in peri-implantitis and therefore a reduction in the failure rate of MSIs. This subject needs further exploration. Minute amounts of other elements were seen: nitrogen, fluorine, sodium, chlorine, magnesium, and potassium. Most of these elements are present in drinking water, foods, mouthwashes, toothpastes, and beverages. A study of retrieved MSIs by Eliades et al8 showed no difference in the Vickers microhardness testing between as-received and retrieved MSIs, implying that no strainhardening phenomena occurred despite the self-drilling process. The SEM and EDX analyses did not provide substantial information on the greater inflammation associated with loosened MSIs. One possibility of the loosening of MSIs could be due to the biofilm formed on metallic implants as reported by Arciola et al44 and Schaer et al45; biofilm formation can be significantly reduced by hydrophobic polycationic coatings. We hypothesized that the loosening of MSIs could be due to biofilm formation on metallic implants leading to microbial attack on surrounding bone and subsequent inflammation. The confirmation of biofilm formation would need an elaborative study, as we envisage in a future study. Thus, the outermost atomic layers of MSIs are critical regions associated with biochemical surface interactions of the implant-tissue interface. This should have a tremendous influence on a high degree of standardization and surface control in the production of MSIs.35 This knowledge will be helpful in exploring possible research approaches for determining the biologic properties of implant materials. CONCLUSIONS

The results of this retrieval analysis of MSIs have suggested the following. 1.

Retrieved MSIs exhibit morphologic surface changes in the form of dullness, blunting of threads and tips, corrosion, craters, and occasional tearing of thin threads.

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3.

4.

The surface elemental composition of retrieved MSIs differs from that of as-received MSIs, with additional elements; the most conspicuous was calcium in the body region (P \0.05). The surfaces of failed MSIs compared with successful MSIs have higher adsorption of iron at all 4 zones (mean, 0.214 weight percent), the source of which can be attributed to inflammation around the MSIs in the bone and gingiva. Although the head and neck regions of retrieved MSIs show cerium in greater proportions (mean, 0.137 weight percent), these findings should be confirmed in a larger sample with adequate power along with other elements such as iron.

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14.

15.

16.

17.

ACKNOWLEDGMENTS 18.

We thank the Electron Microscope Facility of All India Institute of Medical Sciences, New Delhi; and Dr R. M. Pandey, Professor & Head, Biostatistics; Guresh Kumar; and Ashish DU for their contributions to the statistical analyses.

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American Journal of Orthodontics and Dentofacial Orthopedics

Surface deterioration and elemental composition of retrieved orthodontic miniscrews.

This study provides insight into surface and elemental analyses of orthodontic retrieved miniscrew implants (MSIs). The sole purpose was to investigat...
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