Artifact Properties of Dental Ceramic and Titanium Implants in MRI

Key words

peri-implantitis - magnetic resonance imaging - ceramic implant - titanium implant - three-dimensional imaging - artifacts

Introduction

12.4 % of 65 – 74-year-olds have no teeth [1]. Due to the importance of implants for oral rehabilitation after the loss of natural teeth [2], preoperative imaging is required for optimal treatment planning with maximum risk reduction and predictability of long-term success [3] [4]. MRI could play an important role here due to the visualization of soft-tissue structures [5].

The biggest problem with respect implant care is the risk of peri-implant infection. Implant loss [7] is increasingly being seen as a result of the growing prevalence of peri-implantitis [6]. Therefore, early visualization of peri-implant infections is important. The current gold standard for the visualization of implants is based on X-ray methods such as the panoramic radiograph ([Fig. 1a]) and the classic bitewing X-ray ([Fig. 1b, c]).

Fig. 1 OPG a and single-tooth radiograph (b, c) images of a titanium implant in region 42 b and for a ceramic implant in region 32 c.

Although implants can be effectively visualized with these classic methods, relevant information along the direction of projection is lost as a result of the two-dimensional measurement technique. Therefore, studies are increasingly focusing on three-dimensional diagnostic imaging methods [3] [4]. With respect to the prevalence of peri-implant infections and their consequences, the S3 guidelines come to the conclusion that the prevention of peri-implantitis is cheaper than the treatment of the disease. Therefore, the authors of the guidelines feel that three-dimensional imaging (primarily DVT) can be used for the visualization of advanced and complex lesions, for treatment planning and for treatment decisions [8].

However, DVT imaging seems to be problematic with respect to the evaluation of osseointegration. In addition to the radiation exposure for the patient, it is often not possible to evaluate inflammatory processes due to the limited soft-tissue contrast and to visualize the implant interface due to artifacts in the case of both titanium and ceramic implants ([Fig. 2]).

Fig. 2 CBCT representation of the titanium (42, b) and ceramic implant (32, c). Please note the severe long-ranging streak artifacts caused by the implants a.

Due to the high-contrast visualization of soft tissues, MRI represents an attractive radiation-free alternative here [4] [5] [9] [10] [11] [12] [13] [14]. However, the MRI method is limited by its sensitivity to metals and the resulting artifacts [2] [15]. In most cases, titanium implants could not be evaluated, while ceramic implants were artifact-free ([Fig. 3]).

Fig. 3 MRI representation of the titanium (42, red circle in a, arrow in b) and ceramic (32, white circle in a, arrow in c) implant. Please note the only local artifacts caused by the titanium implant and lack of artifacts for the ceramic implant a.

A strong dependence of the resulting artifacts on the dental material and the sequence was observed [14] [16] [17] [18] [19] [20] [21].

To evaluate the applicability of MRI for visualizing an implant after implantation, various three-dimensional MR measurement sequences (spin echo (SE), gradient echo (GE), ultrashort TE (UTE)) with isotropic spatial resolution were compared with respect to artifacts for titanium and ceramic implants in the present study.

Materials and Methods

Implants

In total, 8 (2 ceramic (#1, #8), 6 titanium (#2 – #7)) different implant types were examined (see [Table 1]). In three cases, multiple implants (#3: 7; #6: 3; #8: 6) of the same type were examined, with implants from two different lots being included in cases #3 and #8. To achieve conditions that were as realistic as possible, all implants were removed from sterile packaging and sterilized immediately prior to the experiment. Each implant was embedded in agarose (SERVA^® tablets (Serva, Heidelberg), 0.5 g/tablet, molecular biology grade) in a sealable transparent specimen container and then examined using the standardized MR protocol.

Table 1 Implants (#1 Ziterion, #2 – 8 Bredent).

implant number	model name	implant diameter	implant length
#1	ZI510H ®	5.0 mm	10 mm
#2	bSKY4010 ®	4.0 mm	10 mm
#3 (7 units)	SKY4514 ®	4.5 mm	14 mm
#4	bSKY4012 ®	4.0 mm	12 mm
#5	bSKY3514 ®	3.5 mm	14 mm
#6 (3 units)	SKY4512 ®	4.5 mm	12 mm
#7	bSKY4510 ®	4.5 mm	10 mm
#8 (6 units)	white sky SKY4512C ®	4.5 mm	12 mm

MR – measurement protocol

All data were recorded on a clinical 3 T whole-body MRI unit (Achieva 3 T, Philips Healthcare, Best, The Netherlands). For the measurement, the embedded implants were fixed to a segment of a 2 × 2-channel carotid coil in random orientation. The measurement protocol included spatially isotropically resolved three-dimensional sequences. A T1-weighted turbo spin echo (SE) sequence and a corresponding steady-state gradient echo (FFE) sequence were used as the clinically established sequences. In addition, an ultrashort TE (UTE) sequence was examined as a special technique for reducing metal-induced signal cancellation [21]. Detailed acquisition parameters are provided in [Table 2].

Table 2 Summary of the relevant MR parameters.

measurement parameters	UTE	SE	FFE
FOV RL/FH(mm)	120	120	120
AP(mm)	120	30	60
voxel size RL/FH/AP(mm)	0.5	0.5	0.5
TR/TE (ms)	12/0.14 (3 × oversampled)	419/11 (4 echoes)	5.5/2.0
total scan duration	31 m 41 s	25 m 8 s	2 m 38 s
BW (Hz)	656.5	444.6	1883.2

Data analysis

The sequences and implants were compared based on the measured volumes of the implants including signal cancellation in the acquired volume datasets. These were segmented using a region-growing technique semiautomatically via ITK Snap^® Version 2.2.0. To facilitate segmentation, seed points were manually set in the region of the implants to support the region-growing algorithm. The various implants and measurement techniques were compared by determining the relative error in comparison to the real implant volumes provided by the manufacturers.

Statistical significance was determined using a two-sided paired student’s t-test. Differences with p-values less than 0.05 were considered significant.

Results

The measurements were successfully performed for all implants. [Fig. 4] shows an example of the central layer of a titanium and a ceramic implant visualized with the investigated MR techniques.

Fig. 4 MRI representation of a titanium (#6, a – c) and ceramic (#1, d – f) implant acquired with FFE (a, d), SE (b, e) and UTE (c, f).

Significant artifacts and deformations were observed for all titanium implants. Even if a dependence of the resulting artifacts on the orientation of the implant was observed, it was not possible to evaluate the direct periphery of the implants in any of the examined cases. Extensive artifacts, as observed for example in DVT ([Fig. 2a]), were not seen. Artifacts were limited to the immediate vicinity of the implants.

No artifacts were observed in the case of the ceramic implants and the periphery of the implants was also able to be effectively evaluated. Any limitations are the result of the moderate spatial resolution of 0.5³ mm³.

The quantitative analysis of the implants is summarized in Tables 3 – 7. The direct comparison of the quantified volumes in the MR data with the theoretical values (titanium, [Table 3]; ceramic, [Table 5]) and the resulting relative errors (titanium, [Table 4]; ceramic, [Table 6]) highlight the qualitative impression of the images. Regardless of the measurement sequence, an average relative error of more than 1000 % was observed for the titanium implants. Average errors of only 5 % were seen for the ceramic implants. Among the MR measurement sequences, significant differences were seen between FFE and SE (p < 0.001) as well as UTE and SE (p < 0.01) but not between FFE and UTE (p = 0.47) for the titanium implants. No significant differences were seen for the ceramic implants.

Table 3 Theoretical (actual vol.) and measured (digital vol.) volume for titanium implants resulting from the investigated MR sequences.

impl. no.	actual vol. [mm3]	digital vol. FFE [mm3]	digital vol. SE [mm3]	digital vol. UTE [mm3]
#2	76.39	977.62	1412.27	878.95
#3A_1.Ch	143.73	1840.74	2884.66	1244.22
#3B_1.Ch	143.73	1846.15	4066.83	2620.81
#3C_1.Ch	143.73	2166.51	4200.02	3116.91
#3A_2.Ch	143.73	1628.85	2564.22	2506.02
#3B_2.Ch	143.73	1903.43	2576.62	1294.79
#3C_2.Ch	143.73	2646.00	4790.89	2744.59
#3D_3.Ch	143.73	1706.86	1894.40	2447.09
#4	90.91	1039.95	1354.20	1134.07
#5	80.53	880.08	1210.67	763.50
#6A	122.23	2506.31	2086.87	1638.13
#6B	122.23	2271.29	4327.23	3438.55
#6C	122.23	2281.90	4416.76	1707.26
#7	102.28	976.27	1960.93	989.12

Table 5 Theoretical (actual vol.) and measured (digital vol.) volume for ceramic implants resulting from the investigated MR sequences.

impl. no.	actual vol. [mm3]	digital vol. FFE [mm3]	digital vol. SE [mm3]	digital vol. UTE [mm3]
#1	221.93	249.20	242.19	237.30
#8A_1.Ch	239.69	258.75	247.72	256.14
#8B_1.Ch	239.69	247.60	252.07	257.73
#8C_1.Ch	239.69	257.88	257.86	225.75
#8A_2.Ch	239.69	243.35	226.64	258.86
#8B_2.Ch	239.69	272.93	256.67	255.32
#8C_2.Ch	239.69	251.51	257.97	242.95

Table 4 Relative error for titanium implants resulting from the investigated MR sequences.

impl. no.	error FFE [%]	error SE [%]	error UTE [%]	average error (standard deviation) [%]
#2	1179.85	1748.86	1050.67	1326 (371)
#3A_1.Ch	1180.71	1907.03	765.68	1285 (578)
#3B_1.Ch	1184.48	2729.53	1723.45	1879 (784)
#3C_1.Ch	1407.36	2822.20	2068.62	2099 (707)
#3A_2.Ch	1033.29	1684.08	1643.59	1454 (363)
#3B_2.Ch	1224.33	1692.71	800.86	1239 (446)
#3C_2.Ch	1740.98	3233.30	1809.58	2261 (842)
#3D_3.Ch	1087.56	1218.05	1602.58	1302 (267)
#4	1043.88	1389.54	1147.41	1194 (177)
#5	992.90	1403.43	848.13	1081 (288)
#6A	1950.44	1607.29	1240.17	1599 (355)
#6B	1758.16	3440.15	2713.11	2637 (844)
#6C	1766.84	3513.40	1296.73	2193 (1167)
#7	854.54	1817.28	867.10	1179 (552)

Table 6 Relative error for ceramic implants resulting from the investigated MR sequences.

impl. no.	error FFE [%]	error SE [%]	error UTE [%]	average error (standard deviation) [%]
#1	12.29	9.13	6.92	9.4 (2.7)
#8A_1.Ch	7.95	3.35	6.86	6.1 (2.4)
#8B_1.Ch	3.30	5.17	4.72	4.4 (1.0)
#8C_1.Ch	7.59	7.58	5.81	7.0 (1.0)
#8A_2.Ch	1.53	5.45	8.00	5.0 (3.3)
#8B_2.Ch	10.89	7.09	3.74	7.2 (3.6)
#8C_2.Ch	2.03	7.63	1.36	3.7 (3.4)

The direct comparison between the theoretical implant volume and the MRI measurements is highly significant (p < 0.001) for all titanium implants and measurement sequences. Significant differences for FFE (p < 0.05) and SE (p < 0.05) but not for UTE (p = 0.06) were observed for the ceramic implants.

The means and standard deviation of the implants that were investigated multiple times (#3, #6, #8) are shown in [Table 7]. Significant variation was also seen in the results for the titanium implants that were measured several times. Interestingly, the greatest variations occurred in the SE sequence, while the smallest amount of variation was seen in the FFE sequence.

Table 7 Mean and standard deviation (in parentheses) of the volume and relative error for the titanium (#3, #6) and ceramic (#8) implant series.

means	#3	#6	#8
volume FFE [mm3]	1962 (345)	2532 (132)	255 (10)
volume SE [mm3]	3282 (1067)	3610 (1320)	249 (12)
vol. UTE [mm3]	2282 (725)	2261 (1012)	249 (12)
error FFE [%]	1265 (855)	1825 (108)	5.6 (3.8)
error SE [%]	2183 (1817)	2853 (1080)	6.0 (1.7)
error UTE [%]	1487 (867)	1750 (867)	5.1 (2.4)

Discussion

The use of MRI for the three-dimensional visualization of titanium and ceramic implants and the surrounding structures was examined on the basis of various MR sequences. Interestingly, the greatest variation and also the greatest errors for all implant types were seen in the case of the SE technique. UTE and FFE did not show significant differences. Significant differences were only observed in the case of the titanium implants. This is most likely due to the strong magnetic field interference caused by the titanium implants, which, in connection with the low bandwidth of the excitation and refocusing pulses of the SE sequence, allows only incomplete excitation of the surrounding tissue.

The minimal standard deviation of the ceramic implant results (FFE: 6.5 ± 4.3 %; SE: 6.4 ± 2 %; UTE: 5.3 ± 2.3 %) indicates position and orientation independence of this implant type. In the case of titanium implants, a strong dependence of the artifacts on implant position and particularly orientation was observed as shown by the significant variability of the results (FFE: 1766 ± 348 %; SE: 2157 ± 810 %; UTE: 1398 ± 562 %).

As expected and also proven by other studies [11] [13] [15] [22] [23], all titanium implants caused artifacts, some of which were quite significant, thereby rendering evaluation of the implant shape and the structures near the implant impossible. Therefore, the MRI technique currently cannot be used as an alternative to conventional imaging methods in the region of titanium implants. However, ceramic implants and the immediate vicinity can be visualized clearly and precisely so that MRI can be considered as an alternative method for monitoring the healing process of ceramic implants.

Currently available data

Diagnostic imaging is important for reducing implant risks [24] [25] [26]. The use of OPG for preoperative planning and postoperative assessment of standard titanium implants currently represents the clinical standard [27]. In contrast to other disciplines [3] [4] [10] [11] [12] [28], the use of MRI is limited in dentistry due to the susceptibility to metal-induced artifacts [11] [14] [19]. Metal objects cause artifacts and image distortion in MRI [11] [13] [15] [22]. The resulting artifacts vary based one differences in the susceptibility of the materials being used, the shape and orientation of the object, the material composition, and the magnetic field strength [10] [11] [14] [22] [29] [30].

Although titanium dental implants have been classified as biocompatible for many years and represent the gold standard in dental implantology due to their positive material properties [13] [31] [32] [33], ceramic implants have been having a renaissance in recent years [20] [23] [34] [35]. Various studies have proven excellent osseointegration, high biocompatibility, and a positive tissue response [35] [36] [37] [38] [39]. Moreover, studies have shown a connection between titanium implants and allergic reactions, inflammation, hematological and metabolic toxicity and hypersensitivities to metal components [35] [36] [37] [39]. The new generation of ceramic implants offers new possibilities in the field of implantology.

In an in vitro study, Duttenhofer et al. compared MRI vs. conventional X-ray methods (OPG, DVT and CT) for examining titanium and ceramic implants in order to evaluate the accuracy of the methods for preimplant planning and postoperative follow-ups [27]. They were able to show that the quality of preoperative imaging was the same for all methods. However, significant image distortion in postoperative imaging was seen in the case of titanium implants in contrast to ceramic implants.

Matsuura et al. examined 6 different types of ceramic, pure titanium, and titanium alloys for susceptibility artifacts. The results confirmed the conclusion of other studies that all tested ceramics resulted in much less significant artifacts than the examined metals [40]. They concluded that ceramic is the biomaterial that is best suited for reducing artifacts when using MRI [40].

This study confirmed that titanium implants cause major artifacts in every examined measurement technique [11] [13] [15] [31], while the images of all examined ceramic implants were artifact-free. Therefore, it can thus be assumed that ceramic implants can be visualized in precise detail with MRI. Thus, MRI can be used as an alternative to the gold standard, X-ray imaging, as long as there are no metal objects in the immediate vicinity [27].

Clinical significance

The investigated MRI methods cannot be used to evaluate the periphery of titanium implants. However, the results show that ceramic implants can be precisely visualized with various MRI methods. It can be assumed that MRI can play an increasingly relevant role in the evaluation of implantation results as well as the evaluation of the healing process and the diagnosis of peri-implant complications at least in the case of ceramic implants.

Limitations

The effect of the position and orientation of the implant relative to the direction of the static magnetic field was not systematically examined. However, a significant relationship between titanium implant-induced artifacts and implant orientation can be concluded from the observed variability of the results.

The evaluation method used in this study did not include analysis of possible distortions and it is theoretically possible for distortion of the examined implant with the same volume to occur. This was not observed in the visual assessment of the results but may require further study.

Moreover, the measurement sequences used in this study are not sequences used in the clinical routine. Undersampling (parallel imaging, compressed sensing) was not used to accelerate the process and the geometric isotropic coverage of the measurement volume resulted in unacceptable measurement times for the clinical routine in particular for the spin echo and UTE techniques.

Conclusion

The results of this study showed that MRI technology could be an alternative to conventional radiology, CT and DVT for the evaluation of ceramic implants since, in contrast to titanium implants, both the ceramic implant and the peri-implant region can be effectively visualized in vitro with MRI. Thus, it is possible to obtain relevant information for diagnosis and treatment decisions in the case of peri-implant complications without radiation exposure and with improved visualization of the surrounding soft tissue via the three-dimensional visualization of the implant periphery.

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