Introduction

Dental practitioners are often caught in a dilemma when they have to decide between immediate and early implant placement after tooth extraction. It is prudent to plan early implant placement when the morphology of the sight prevents an optimal immediate implant placement, or a thin soft tissue biotype; also, a thin bone wall phenotype would make the implant therapy unpredictable due to the resorption of the buccal bony plate. Mature wound closure and a compensatory soft tissue thickening at 6–8 weeks combined with contour augmentation makes implant placement more predictable.1  The early implant placement is also recommended in the case of inflammation of the bone, for example, apical periodontitis associated with the extracted tooth.24  This is in line with the definition of type 2 implant placement protocol proposed at the 3rd ITI Consensus Conference in 2003, which refers to the placement of an implant after substantial soft tissue healing has taken place.2  Based on empirical evidence, complete soft tissue healing at the extraction site takes 4 to 8 weeks. Obviously, that broad time interval provides for deviation due to the method of tooth extraction and individual differences in pace of healing. Only a few studies placed postextraction soft tissue healing under scrutiny.5,6  In humans, complete re-epithelialization of the extraction wound takes place at 24–35 days.7  At the same time, it is not known when the connective tissue of the submucosa with an adequate vasculature emerges, which is a prerequisite for the survival of a subsequent surgical flap.

Any objective method of measurement of the time required for soft tissue healing adjacent to the extraction wound would allow for administration of the subsequent treatment steps without unnecessary time loss or delay for better predictability of treatment outcomes. We assume that the optimal healing time for early implant placement coincides with the recurrence of preoperative, that is, resting blood flow values at the site.

Monitoring microcirculation is an acknowledged method of tracking wound healing. Studies in human subjects811  show that blood circulation and capillary density in the mucoperiosteal flap return to the baseline during the third postoperative week on average; however, the actual time needed is highly dependent on the surgical technique used and individual differences.

Laser speckle contrast imaging (LSCI) is an optical method of superior reproducibility due to its real-time 2D image functionality allowing for simultaneous monitoring of even the entire area of a flap12  compared to laser Doppler flowmetry,13  which was widely used earlier for blood flow measurements. LSCI exploits the random speckle pattern, which is generated when tissue is illuminated by laser light. Movements within a tissue, such as blood flow, cause changes in the speckle pattern of that tissue and these changes, that is, fluctuations in intensity blur the image captured by the charge-coupled device camera, leading to a reduction in local speckle contrast. As a result, blood flow velocity distributions are coded as speckle contrast variations.14  In previous studies, our working group has found that LSCI is suitable also for mapping microvascular blood flow in the gingiva.11,15,16 

In the present study, LSCI was used for monitoring blood circulation in the gingival area close to the extraction site following surgical tooth extraction in order to determine—based on a previously developed methodology15—the optimal time for surgery in preparation for early implant placement.

Materials and Methods

Case history, diagnosis, and treatment plan

A 28-year-old male patient came to our clinic to have his maxillary left second premolar with a fractured crown restored. The medical history of the patient did not reveal any systemic disease, medication, or smoking. The patient's dental history and the intraoral examination revealed that the filling placed during previous root canal therapy was not suitable to prevent fracture, which led to loss of the palatal cusp (Figure 1a). The intraoral X ray (Figure 1b) shows a separated instrument into the root canal, overfilling, and periapical radiolucency. It was also observable that distally the intact tooth structure was on a level with the marginal bone. Based on the foregoing, tooth extraction and implant restoration was our recommended treatment plan, which the patient accepted. Prior to surgery, the patient underwent supragingival calculus removal and received oral hygiene instructions. The patient received exhaustive information on the treatment, possible complications such as sinus perforation, infection, dry socket, fracture of the surrounding bone, failed osseointegration, as well as about the blood flow measurements to be performed. The measurement series was carried out in accordance with the Declaration of Helsinki. Ethical approval was granted by the National Healthcare Services Center of Hungary (approval number: 034310/2014/OTIG).

Figures 1–4

Figure 1. Baseline image from an occlusal view before treatment (a) and intraoral X ray (b) of the maxillary left second premolar. Figure 2. Elevation of a mucoperiosteal flap upon tooth extraction (a) and 2 months later upon implant placement (b). Figure 3. Cone beam computerized tomography image 2 months after tooth extraction (a) and intraoral X ray after implant placement (b). Figure 4. Graphical representation and designation of the regions defined for the evaluation of blood flow measurements. Occlusal view (a) region of interest (ROI) A: extraction wound; ROI B: 1 mm wide circular area around ROI A; ROI C: 1 mm wide circular area around ROI B; ROI D: region covering the rest of the gingiva. Buccal view (b) ROI E: a region including a 2 mm wide section of the marginal gingiva; ROI F: a 2 mm wide apical extension to ROI E; ROI G: a 2 mm wide apical extension to ROI F, lying at the mucogingival junction.

Figures 1–4

Figure 1. Baseline image from an occlusal view before treatment (a) and intraoral X ray (b) of the maxillary left second premolar. Figure 2. Elevation of a mucoperiosteal flap upon tooth extraction (a) and 2 months later upon implant placement (b). Figure 3. Cone beam computerized tomography image 2 months after tooth extraction (a) and intraoral X ray after implant placement (b). Figure 4. Graphical representation and designation of the regions defined for the evaluation of blood flow measurements. Occlusal view (a) region of interest (ROI) A: extraction wound; ROI B: 1 mm wide circular area around ROI A; ROI C: 1 mm wide circular area around ROI B; ROI D: region covering the rest of the gingiva. Buccal view (b) ROI E: a region including a 2 mm wide section of the marginal gingiva; ROI F: a 2 mm wide apical extension to ROI E; ROI G: a 2 mm wide apical extension to ROI F, lying at the mucogingival junction.

Tooth extraction

Due to the extensive loss of coronal tooth structure, surgical tooth extraction was performed. After administering local anesthesia (2 × 2 mL lidocaine-adrenaline 20 mg/0.01 mg/mL injection) intrasulcular incisions were made and the papillae were split to elevate a full-thickness mucoperiosteal flap (Figure 2a). Tooth extraction was performed gently, using extraction forceps and avoiding any damage to the surrounding bone structure. Approximal horizontal mattress sutures (5/0 Dafilon, B. Braun, Hessen, Germany) were used for reapproximation of the flap, but no complete closure was achieved. In accordance with a previously developed protocol, after surgery, the patient was instructed to rinse twice a day with a mouthwash containing chlorhexidine (Corsodyl 0.2%, GSK, Brentford, UK) for a week. No antibiotic was prescribed. The sutures were removed after a week.

Implant placement

In our case, the root apex lay immediately below the cortical bone of the sinus (Figure 1b). Therefore, sufficient primary stability of an immediate implant could not be achieved by osteotomy beyond the apical end of the root and due to the discrepancy between geometry of the socket and implant. This led to implant placement 2 months later, after the formation of soft tissue over the extraction wound and partial bone fill of the alveolar socket (Figure 3a).

The surgery was performed under local anesthesia (2 × 2 mL lidocaine-adrenaline 20 mg/0.01 mg/mL injection). Access to the alveolar process was gained through a mucoperiosteal flap elevated by a slightly buccally placed crestal and by intrasulcular incisions extending to 1/3 of the adjacent teeth (Figure 2b). After preparing the osteotomy, an Astra OsseoSpeed TX straight implant (Dentsply Implants, Mannheim, Germany) of 4.0 mm in diameter, 8 mm in length was placed at an insertion torque of 25 Ncm for primary stability. Since the buccal bone had appropriate dimensions, no bone augmentation was necessary. Based on satisfactory primary stability and the appropriate dimensions of the keratinized gingiva, we opted for transgingival healing, with the application of a healing cap of 4.5 mm in diameter. To facilitate optimal flap adaptation and to support subsequently developing interdental soft tissue, small rotated pedicle flaps created from the palatal half were used for closure of the wound with vertical mattress sutures (5/0 Dafilon, B. Braun). No antibiotic was prescribed. Sutures were removed after an uneventful healing period of a week.

Soft tissue blood flow measurements

Wound healing and soft tissue alterations were monitored visually and by measuring blood flow. Soft tissue blood flow was monitored by a PeriCam PSI HR laser speckle contrast imaging device (Perimed AB, Stockholm, Sweden). Blood flow was measured at the surgical site before extraction (baseline) and on days 1, 3, 5, 7, 11, 14, 20, 31, 42, and 62 postextraction, then after implant placement on days 1, 4, 7, 20, and 498 (ie, on days 63, 66, 82, and 562 postextraction).

We have described our methodology of gingival blood flow measurement by LSCI in detail in previous studies.11,15  Briefly, measurements were taken in the morning, at a temperature of 26°C in a quiet room. Blood pressure was measured (Omron M4, Omron Healthcare Inc, Kyoto, Japan) after a 15-minute period of rest in supine position in a dental chair. Blood pressure was recorded also at the end of the blood flow measurements. Soft tissue in the oral cavity was retracted using a dental mirror to make the surgical site visible. Buccal and occlusal snapshots were taken by the LSCI device at an interval of 2 seconds, the former directly, the latter using a dental photographic mirror. The Pimsoft software (Perimed AB) was used for the recording, photographic and graphic display, and evaluation of the measured values. Blood flow was expressed in laser speckle perfusion units (LSPU), an arbitrary measurement unit.

During evaluation, identical regions of interest (ROI) were defined—for both surgical interventions—on all LSCI recordings (Figure 4). On occlusal images, ROI A covers the extraction wound, ROI B and C represent concentric regions of a width of 1 mm each around the extraction site, and ROI D, the areas more distant to the wound. On direct buccal images, 2 mm high regions, ROI E, F, and G were defined from the marginal gingiva to the vestibule. ROI G lies already at the mucogingival junction. ROI D of the occlusal and ROI E of the buccal images overlap.

Statistics

Blood flow was measured several times on each day of examination. According to our previous studies,11,15  the interday reproducibility of LSCI measurements in the gingiva may be significantly improved by intrasession repetitions. When comparing blood flow values measured on different days, we also relied on a previous observation15  that a change in blood flow between 2 measurements performed on 2 different days may be established with 95% confidence if the later measurement represents a decrease to 79% or an increase to 127% of the earlier measurement. Soft tissue healing time was estimated based on the regularity of 2 subsequent blood flow measurements, or, when baseline blood flow was known, based on blood flow values' return to the baseline.

Results

The surgical extraction wound healed without complications. Figure 5 clearly shows that as healing of the soft tissue progressed, the area affected by ischemia after tooth extraction began to shrink concentrically already after day 3 and evolved into a homogeneous hyperemic zone by day 20. It was also from day 20 that epithelialization of the extraction wound could be considered complete.

Figure 5

Photographs in occlusal view and the corresponding laser speckle contrast images taken at priority time points of the study.

Figure 5

Photographs in occlusal view and the corresponding laser speckle contrast images taken at priority time points of the study.

On the first day postextraction, there was a significant drop in gingival blood flow around the extraction wound—that is, the distal area of the mucoperiosteal flap—compared to the baseline (Figure 6a). The occlusal images revealed similar blood flow curves in the buccal and palatal regions. These curves were therefore consolidated. Ischemia lasted 7 days in ROI B and 5 days in ROI C, followed by a hyperemic period of 3 weeks in both regions. At 2 mm apically from the edge of the flap (ROI D), no ischemia was observed, and from day 5 hyperemia also occurred here for 3 weeks (Figure 6a). In the area of the extraction wound (ROI A), clearly significant blood flow was measured on day 14, comparable to the degree of hyperemia in the adjacent regions. In occlusal regions (ROI A to D) the blood flow values measured on day 62 postextraction did not differ significantly either from the values measured on day 42 (ROI A: 88%, ROI B: 95%, ROI C: 103%, and ROI D: 111%) or from baseline values (ROI B: 100%, ROI C: 89%, and ROI D: 89%).

Figures 6 and 7

Figure 6. Gingival blood flow (GBF) expressed in laster speckle perfusion unit (LSPU) over time from baseline measurements (bsl) to day 62 postextraction. In the occlusal view (a) region of interest (ROI) A: extraction wound; ROI B: 1 mm wide circular area around ROI A; ROI C: 1 mm wide circular area around ROI B; ROI D: region covering the rest of the gingiva. In the buccal view (b) ROI E: a region including a 2 mm wide section of the marginal gingiva; ROI F: a 2 mm wide apical extension to ROI E; ROI G: a 2 mm wide apical extension to ROI F, lying at the mucogingival junction. Figure 7. Blood flow (in LSPU) over time—from the measurement immediately preceding implant placement (bsl2) to the 1-year follow-up. In the occlusal view (a) ROI B: 1 mm wide circular area around the healing cap; ROI C: 1 mm wide circular area around ROI B; ROI D: region covering the rest of the occlusal gingiva. In the buccal view (b) ROI E: a region including a 2 mm wide section of the most coronal gingiva; ROI F: a 2 mm wide apical extension to ROI E; ROI G: a 2 mm wide apical extension to ROI F, lying at the mucogingival junction.

Figures 6 and 7

Figure 6. Gingival blood flow (GBF) expressed in laster speckle perfusion unit (LSPU) over time from baseline measurements (bsl) to day 62 postextraction. In the occlusal view (a) region of interest (ROI) A: extraction wound; ROI B: 1 mm wide circular area around ROI A; ROI C: 1 mm wide circular area around ROI B; ROI D: region covering the rest of the gingiva. In the buccal view (b) ROI E: a region including a 2 mm wide section of the marginal gingiva; ROI F: a 2 mm wide apical extension to ROI E; ROI G: a 2 mm wide apical extension to ROI F, lying at the mucogingival junction. Figure 7. Blood flow (in LSPU) over time—from the measurement immediately preceding implant placement (bsl2) to the 1-year follow-up. In the occlusal view (a) ROI B: 1 mm wide circular area around the healing cap; ROI C: 1 mm wide circular area around ROI B; ROI D: region covering the rest of the occlusal gingiva. In the buccal view (b) ROI E: a region including a 2 mm wide section of the most coronal gingiva; ROI F: a 2 mm wide apical extension to ROI E; ROI G: a 2 mm wide apical extension to ROI F, lying at the mucogingival junction.

In buccal regions (ROI E, F, and G) hyperemia was observed from day 5 for 3 weeks, without any ischemic period preceding it (Figure 6b). There was no significant change in the blood flow values measured on day 62 in the buccal regions as compared to day 42 (ROI E: 85%, ROI F: 85%, and ROI G: 89%) or baseline values (ROI E: 97%, ROI F: 116%, and ROI G: 116%). There is a clear increase in blood flow values from the edges of the flap towards its base (Figure 6b). Hyperemia arises first at the base of the flap (in ROI G) and spreads gradually toward the edges of the flap, reaching the extraction wound the latest.

Wound healing after implant placement was also free of complications. Unlike in the case of the flap created for tooth extraction, no pronounced ischemia occurred in either of the regions (day 63 vs. day 62: ROI B: 84%, ROI C: 118%, and ROI D: 166%; Figure 7a). Instead, all regions were affected by hyperemia after implantation (day 63–82) with various time and degrees. During the 1-year follow-up no measurements were taken in ROI B and C as the crown obstructed the view. In ROI D and E, blood flow values did not differ significantly from those measured on day 20 postoperatively (day 82) (ROI D: 96%, ROI E: 89%), whereas in ROI F and G they fell below day 20 values (ROI F: 78%, ROI G: 78%; Figure 7b). As compared to the results of the measurement taken immediately before implant placement (day 62), blood flow values were similar in all regions (ROI D: 111%, ROI E: 124%, ROI F: 124%, and ROI G: 118%).

Discussion

The premolar region is best suited for immediate implant placement due to the ease of positioning the implant properly from a prosthetic point of view, favorable anatomic conditions and lower aesthetic risk as compared to the front region. In our case, however, satisfactory primary stability could not have been achieved upon immediate implant placement due to inadequate vertical bone dimension. Therefore, we opted for a 2-stage treatment plan: tooth extraction followed by early implant placement. In order to assess the optimal timing of the second surgical intervention, wound healing was monitored by an LSCI device.

After surgery, first ischemia, then hyperemia occurred in the distal part of the mucoperiosteal flap. Moving gradually toward the base of the flap, ischemia was less frequent and, in line with general observations in the literature,10,11,17,18  only hyperemia occurred, which showed a difference in terms of duration. Blood flow became stable in the entire area of the extraction wound and the mucoperiosteal flap elevated as part of the surgery after the 6th week postextraction. This indicates that the minimum recommended healing period of 4 weeks for early implant placement would not have been sufficient in this case for soft tissue to heal completely. After the 6th week, however, implant placement could have been performed freely. The healing period may be shorter following atraumatic tooth extraction without flap elevation. Primary closure with a repositioned flap technique would probably shorten the healing process due to early epithelial closure and a lower rate of granulation tissue formation.19  Revascularization of the flap, however, may be delayed due to the periosteal incisions and flap advancement.20 

There is very little data available on the timeline of revascularization of the gingiva after extraction.21  A human study involving a high number of cases should be conducted to define the effect of socket dimensions, site location, as well as the flap procedure on the time required for the stabilization of blood flow. At the same time, as individual differences seem to have an impact, monitoring at individual level may be more useful for the optimal timing of a second intervention, when necessary. As a noninvasive method of excellent reliability and reproducibility,15  LSCI would be suitable for monitoring the microcirculation of the oral mucosa in everyday clinical practice. Limitations of application include that LSCI devices are expensive, massive, and allow for measurements only in direct view, which prevents access to all areas of the oral cavity. Recently, the prototype of a miniature LSCI device has been developed for gingival measurements22 ; however, it measures only a small area of the gingival papilla by transillumination, taking advantage of the lack of hard tissue. A miniaturized LSCI having a similarly wide angle and high spatial resolution as the one used in our study (PeriCam PSI HR) would be useful for routine blood flow measurements in flap surgery.

Interestingly, unlike in the case of the flap created for tooth extraction, no ischemia was observable at the distal part of the mucoperiosteal flap elevated upon implant placement, and the arising hyperemia was also milder. A possible explanation for this is vascular reorganization following the first intervention that ensured perfusion in the distal areas of the flap exposed to ischemia. As a result, blood flow decreased to a lesser degree during the second intervention. Artificially induced ischemia as angiogenic stimulus is referred to as the “surgical delay procedure” in plastic surgery. The beneficial effects of the delay procedure on the vasculature is observable after six days and it continues up to the 80th day.23  Partial flap elevation as a preliminary procedure enhances circulation in the distal part of the subsequent definitive flap not only through decreased vascular resistance as a result of anatomical and physiological changes (vascular reorganization, angiogenesis, and vasodilation) but also by reduction of the steal effect induced by reactive hyperemia in the proximal part of the flap.24 

Conclusions

Blood flow measurements in the gingiva using LSCI, in combination with the statistical methodology we have developed, seem to be a promising tool for routine monitoring of surgical flaps under clinical conditions. Based on the changes in flap perfusion monitored by LSCI the optimal timing of early implant placements may be assessed individually.

Abbreviations

    Abbreviations
     
  • GBF

    gingival blood flow (measured in laser speckle perfusion unit)

  •  
  • LSCI

    laser speckle contrast imaging

  •  
  • LSPU

    laser speckle perfusion units

  •  
  • ROI

    region of interest

Acknowledgment

This study was funded by the Hungarian Scientific Research Fund (OTKA K112364).

Note

All authors declare that they have no conflicts of interest.

References

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