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Basic and Clinical Research

Two-Dimensional Real-Time Blood Flow and Temperature of Soft Tissue Around Maxillary Anterior Implants

Nakamoto, Tetsuji DDS, PhD*; Kanao, Masato DDS; Kondo, Yusuke DDS, PhD; Kajiwara, Norihiro DDS; Masaki, Chihiro DDS, PhD; Takahashi, Tetsu DDS, PhD§,¶; Hosokawa, Ryuji DDS, PhD#

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doi: 10.1097/ID.0b013e318272fe81
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Abstract

It has been proposed that well-harmonized interface conditions between soft tissue and prostheses are necessary for successful prosthodontic treatment.1–3 However, most of the methods for evaluating gingivae and assessments are dependent on the practitioner’s skill level.4 Such evaluation is much more important for implant treatment because this treatment passes through both the jawbone and oral mucosa or gingiva. A clinical trial has been proposed to evaluate marginal bone by computed tomography scan analysis,5 but there is a rising need for soft tissue diagnosis.

Noncontact and noninvasive laser Doppler flowmetry (LDF) analysis was developed to evaluate the blood flow of marginal tissue.6,7 When an infrared laser is exposed to red blood cells in microvessels, reflection and scattering occur, and Doppler shift causes a frequency change between the incidence and reflection in proportion to blood flow. This method has been introduced in dentistry, revealing the relationship between periodontal disease and blood flow in gingival,8 blood flow recovery process analysis in periodontal surgery,9,10 and the relationship between smoking and gingival blood flow.11,12 It has also been applied to orthopedics to evaluate blood flow in joints,13–15 to evaluate the effect of postoperative joint surgery,16 and to diagnose rheumatoid arthritis.17 LDF has many advantages; however, because it can only detect a very narrow focal area (approximately 1 mm2) at one time, it is impossible to simultaneously compare different areas, and 2-dimensional imaging analyses were required to address this problem. Recently, laser speckle imaging (LSI) was developed, the basis of which is the same as that of LDF: irradiation with an infrared laser and rapid-scanning speckle imaging to create a blood flow image.18,19 This blood flow imaging analysis made it possible to simultaneously compare multiple different spots both quantitatively and qualitatively.

Blood flow analysis with LSI has also been clinically developed in trials involving brain surgery and peripheral perfusion in diabetes. Additionally, it was developed experimentally as a method for evaluating blood flow in the orofacial area during mastication in the rat masseter muscle, which revealed hemodynamics during rest and sympathetic and parasympathetic stimulation.20 As previously described, the nature of blood flow in gingival tissue is often controversial in dentistry; however, LSI measurement has not been applied.21 This study focused on the gingiva and mucosa surrounding anterior implants and captured thermographs to elucidate the relationship between temperature and blood flow because peri-implant soft tissues are always described as having lower blood flow because of the lack of blood supply from the periodontal ligament.22

Materials and Methods

Subjects

This study was performed under the approval of the Ethics Committee of Kyushu Dental College (No. 10–25). Subjects were chosen from those who had undergone implant placement in the anterior maxilla at Kyushu Dental College Hospital and showed good prognosis, no signs of surrounding bone resorption with a follow-up dental x-ray, and no signs of soft-tissue inflammation. Patients were given sufficient explanation, and they then signed a consent form. Those who had transplanted soft tissue surrounding the implant were excluded because it might affect blood flow. Those who had systemic disease such as diabetes or blood/blood vessel disease were also excluded. A total of 20 subjects were included in the study (mean age, 58 y; range, 18–86 y; 9 men and 11 women). All underwent placement of rough-surfaced titanium implants (Nobel Biocare, Astra Tech, or Straumann) and were divided into 2 groups: implant placement without bone grafting (10 subjects) and with bone grafting (10 subjects). All profiles are summarized in Table 1. All metal materials, like titanium screw pins and mesh, used for bone grafting were removed before implant placement surgery.

Table 1
Table 1:
The Surgical and Prosthetic Profile of the Subjects

Blood Flow and Surface-Temperature Imaging

Blood flow was monitored with a 2-dimensional blood flow analysis machine using infrared LSI (780 nm) (OZ-1; Omegawave, Tokyo, Japan); its effective measuring depth was within 1 mm of the surface. A CCD camera was set at a right angle to the buccal surface at a 25-cm distance, and 10 images were obtained from each subject. Subjects were asked to wear goggles (YL331; Yamamoto Kogaku Co. Ltd., Higashiosaka, Japan) to avoid possible discomfort in their eyes.

Surface temperature was then monitored by a thermograph (Thermo GEAR; NEC Avio, Tokyo, Japan) at a 10-cm distance to obtain 4.3-cm high and 5.7-cm-wide imaging. Additionally, a spot thermometer (Thermo-Hunter PT-7LD; Optics Co., Ltd., Ohtsu, Japan) was used to verify the temperature from the thermograph.

Subjects were asked to keep quiet on the dental chair for at least 10 minutes before each measurement. Blood flow imaging and temperature measurements were then performed. Additionally, oral photos were taken to superimpose the LSI and thermograph.

Data Analysis

Ten-pixel regions of interest (ROIs) were set on the buccal-free gingiva, attached gingiva, interdental papilla, and implant-dental papilla for blood flow imaging as shown in Figure 1. Temperature data were also obtained from the thermograph in reference to the ROI on the blood flow images.

Fig. 1
Fig. 1:
Examples of acquired images: (A) oral photo (#12 is an implant-supported prosthesis); (B) blood flow image—the color scale shows the blood flow from 0 mL·min−1 per 100·g tissue (dark blue) to 64 mL·min−1 per 100·g tissue (red). (C) Thermograph: the color scale shows the surface temperature from 32°C (dark blue) to 37.5°C (red). (D) Regions of interest 1) interdental papilla, 2) free gingiva, 3) attached gingiva, 4) dental-implant papilla, 5) free gingiva (implant), and 6) attached gingiva (implant). (E) Radiograph.

The paired t test was used for the comparison between natural teeth and implants of the subjects. Analysis of variance (ANOVA) with Tukey post-hoc test was used for the comparison between subjects. P-values <0.05 were considered statistically significant.

Results

Blood flow and surface temperature surrounding natural teeth and implants were successfully measured with LSI and thermography, respectively. When all anterior implants with and without bone grafts were considered, blood flow around implants, compared with the adjacent natural teeth, was lower in free gingiva (tooth: 23.6 ± 6.1 mL·min−1 per 100·g tissue; implant: 19.1 ± 7.0 mL·min−1 per 100 g tissue; P = 0.00342) and attached gingiva (tooth: 24.4 ± 6.9 mL·min−1 per 100 g tissue; implant: 19.3 ± 6.4 mL·min−1 per 100 g tissue; P = 0.00070). On the other hand, surface temperature was higher in tissue surrounding implants for all dental papilla (tooth: 34.6°C ± 1.2°C; implant: 35.0°C ± 1.1°C; P = 0.0044), free gingiva (tooth: 34.6°C ± 1.1°C; implant: 35.1°C ± 1.2°C; P = 0.000014), and attached gingiva (tooth: 34.4°C ± 1.1°C; implant: 35.0°C ± 1.1°C; P = 0.00069).

When absolute values for both LSI and temperature were compared between subjects and statistically analyzed using multiple comparisons with ANOVA, the difference between the groups was unclear because the values varied by patient. It was therefore decided to compare natural teeth and implants within patients.

Blood Flow and Surface Temperature Around Implants Without Grafting

All blood flow and surface temperature data around implants without grafting with respect to each region are shown in Figure 2. The average blood flow at the dental papilla in an adjacent tooth was 22.7 ± 6.6 mL·min−1 per 100 g tissue, whereas that at the implant-dental papilla was 22.5 ± 7.4 mL·min−1 per 100 g tissue; no significant difference between the 2 was observed (Fig. 2, A). The surface temperature was a bit higher at the implant-dental papilla (tooth: 34.7°C ± 1.2°C; implant: 35.0°C ± 1.2°C), but the difference was not significant (P = 0.0.65 by paired t-test) (Fig. 2, B). The blood flow in the free gingiva was higher in the free gingiva of adjacent teeth compared with that of the implants, but the difference was not significant (tooth: 23.6 ± 6.3 mL·min−1 per·100 g tissue; implant: 19.5 ± 7.4 mL·min−1 per 100 g tissue; P = 0.0857) (Fig. 2, C). On the other hand, the surface temperature was slightly but significantly higher in tissue around implants (tooth: 34.7°C ± 1.2°C; implant: 35.0°C ± 1.3°C; P = 0.00819) (Fig. 2, D). The blood flow at the attached gingiva was marginally significantly lower around implants (tooth: 23.9 ± 6.1 mL·min−1 per 100 g tissue; implant: 19.3 ± 6.3 mL·min−1 per 100 g tissue; P = 0.0468) (Fig. 2, E). The surface temperature at implant-attached gingiva was significantly higher (tooth: 34.3°C ± 1.1°C; implant: 35.0°C ± 1.4°C; P = 0.00593) (Fig. 2, F).

Fig. 2
Fig. 2:
Soft-tissue blood flow and temperature around natural teeth versus implants without bone grafting. Blood flow from LSI (left panels) and surface temperature from thermograph (right panels) in interdental papilla (implant-dental papilla) (A and B), free gingiva (C and D), and attached gingiva (E, F) was compared between natural teeth and implants. n.s., not significant, *P < 0.05, **P < 0.01 with paired t test.

Blood Flow and Surface Temperature Around Implants With Bone Grafting

All blood flow and surface temperature data around implants with bone grafting with respect to each region are shown in Figure 3. The average blood flow at the dental papilla in an adjacent tooth was 26.2 ± 6.5 mL·min−1 per 100 g tissue, whereas that at implant-dental papilla was 22.5 ± 5.1 mL·min−1 per 100 g tissue; this difference was significant (P = 0.0254) (Fig. 3, A). The surface temperature was significantly higher at the implant-dental papilla (tooth: 34.6°C ± 1.3°C; implant: 35.1°C ± 1.0°C; P = 0.0378, paired t test) (Fig. 3, B). The blood flow of the free gingiva was significantly lower in implant-supported free gingiva than in that of adjacent natural teeth (tooth: 23.5 ± 6.4 mL·min−1 per 100 g tissue; implant: 18.8 ± 7.0 mL·min−1 per 100 g tissue; P = 0.0198) (Fig. 3, C). On the other hand, the surface temperature was apparently higher at implant-placed tissue (tooth: 34.5°C ± 1.1°C; implant: 35.2°C ± 1.0°C; P = 0.000545) (Fig. 3, D). The blood flow at attached gingiva was significantly less in implants (tooth: 24.9 ± 7.9 mL·min−1 per 100 g tissue; implant: 19.2 ± 6.9 mL·min−1 per 100 g tissue; P = 0.00805) (Fig. 3, E). The surface temperature at attached gingiva around implants tended to be higher but was not significantly different (tooth: 34.5°C ± 1.1°C; implant: 34.9°C ± 0.8°C; P = 0.0606) (Fig. 3, F).

Fig. 3
Fig. 3:
Soft-tissue blood flow and temperature around natural teeth versus implants with bone grafting. Blood flow from LSI (left panels) and surface temperature from thermograph (right panels) in interdental papilla (implant-dental papilla) (A and B), free gingiva (C and D), and attached gingiva (E and F) was compared between natural teeth and implants. n.s., not significant, *P < 0.05, **P < 0.01, and ***P < 0.0001 with paired t test.

Discussion

LSI was developed to improve single-spot LDF18,19 and has been clinically applied to cerebrovascular surgery,23–25 skin diseases,23–25 and blood recovery from burn injury.26 It is reported that both LSI and thermography as reproducible measurements, and there is excellent correlation between them.27 By combining LSI with thermography, we evaluated differences between soft tissue around implants and that around natural teeth and the effects of bone grafting on soft tissue.

Blood flow analysis with single-spot LDF has been experimentally used to evaluate gingiva in periodontal disease.8–12 The dental papilla has a higher blood flow than does the free gingiva in a resting state in healthy subjects.8 The same results were found in this imaging study; the tendency was much clearer in tissue surrounding implants. It is noteworthy that the probes had to be placed properly for single-spot LDF in most previous studies, but LSI was captured easily from the front at a 25-cm distance with almost identical results, suggesting that this method could become an effective tool for the assessment of periodontal and/or soft tissue around implants. Mavropoulos et al.12 reported that gingival blood flow in a resting state was significantly lower in patients with chronic periodontal disease than in young healthy subjects. In the present study, soft tissue around implants showed decreased blood flow compared with periodontal tissue in adjacent natural teeth, but no clinical signs were observed (pocket depth < 2 mm, no bleeding on probing). This suggests that tissue surrounding implants is stable but has reduced blood flow, even when there is no chronic inflammation.

Interestingly, soft tissue around implants with bone grafting was significantly reduced at all dental papillae, free gingiva, and attached gingiva. This might suggest the difficulty of maintaining a long-lasting emergence profile for maxillary anterior implants, especially in bone graft patients and also suggests the importance of existing bone quality to maintain blood flow.

Surface blood flow reportedly increases in proportion to surface temperature to some extent.28,29 The researchers for this project first predicted a decrease in gingival surface temperature around implants because of the decrease in blood flow, but the opposite phenomenon (higher temperature around implants) was observed. One possible explanation for this is that implants were connected to a deep part of the maxilla by materials with high thermal conductivity or high thermal content. A study on gingival surface temperature reported that thermal properties are different in periodontitis with higher temperature associated with inflammation.30,31 However, this is not the case in tissue surrounding implants.

Conclusions

In conclusion, (1) implant-surrounding tissue has less blood flow as compared with adjacent natural teeth, especially around implants with bone grafting. (2) The surface of implant-surrounding tissue has higher temperature when compared with adjacent natural teeth, especially in the neck and cervical areas of the bone-grafted implants. Because the reduction in blood flow may make it difficult to achieve a successful long-lasting emergence profile,32–34 these 2 measurements might become useful techniques to evaluate not only natural teeth but also soft tissue supporting implants. Future studies will be needed to compare healthy implant-surrounding tissues and inflammation in the peri-implant region.

Disclosure

The authors do not have any financial interests in any of the products mentioned in this article.

Acknowledgments

This work was supported by KAKENHI (22390369).

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Keywords:

blood flow; laser speckle imaging; thermograph; bone grafting

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