Introduction

Dental radiology is a fundamental tool that aids the dentist in performing accurate diagnoses and treatment planning, conducting optimal treatment procedures, and in patient maintenance during treatment follow-ups.1  Radiographic images can reveal otherwise-hidden, internal hard-tissue structures such as bone and teeth. It is impossible to treat patients using modern dentistry techniques when dental radiography is not available. Many kinds of imaging modalities have been introduced for optimal applications, depending on the radiation dose, area of interest, field of view, and required image resolution. Not only plain X rays such as periapical views and bitewing images but also panoramic radiographs are used as basic screening tools. Dental cone-beam computed tomography (CBCT) has recently become an important technique in the dental office for definite and detailed analyses of 3D craniofacial structures such as dental implants, preoperative evaluations of bone graft surgery,2  impacted teeth, and orthodontic treatment.3  The main advantage of CBCT, which is continuing to increase in dentistry, is that it allows for 3D visualizations of craniofacial hard tissues, thus ensuring correct diagnoses and treatment planning.1 

Helpful as it can be, dental radiography still has several shortcomings. The main concern is radiation exposure. Even though the radiation dose in dentistry is relatively low compared to that in conventional medical radiology or medical computed tomography (CT), it is still an important issue, especially when it comes to CBCT,4,5  with many studies focusing on determining the optimal radiation dose in CBCT. The second problem of dental radiography is its limitation in soft-tissue analysis. Some soft-tissue shadows may be evident in dental radiography, but in most such cases, these shadows do not have any clinical significance in evaluations of the masticatory muscles, vessels, or nerves. Magnetic resonance imaging (MRI) may be used for these structures, but its utilization is limited because of its low cost-effectiveness. The third problem is that these image modalities provide only static images, meaning that clinicians cannot evaluate real-time clinical features within regions of interest.

Ultrasonography (US) is very widely used in the medical field for diagnoses involving soft tissues of the human body. US transmits ultrasound signals and is generally performed by holding a special probe in contact with the skin close to the target area. The probe also detects ultrasound echoes that are reflected, depending of the characteristics of the underlying tissue. These reflected echoes are displayed as an image in real time. The procedure is simple, comfortable, free of radiation, and can be used for human body-surface structures such as the breast, thyroid, and muscles. US has also been used in various craniofacial soft-tissue evaluations, such as of the masseter muscle,68  neck lymph nodes,9  temporomandibular joint,10,11  and salivary glands.12  However, for US to be applied in the dental field, the major obstacle is the design of the probe. The probe needs to be in contact with tissue as close as possible to the target area. Yet no intraoral probe for oral surgery has been specially designed to fit the curved and soft oral mucosal area, especially the palatal vault.

It is well known that maintaining oral hygiene around dental implants is critical for a long-term successful outcome. The attached mucosa around an implant plays a significant role in oral hygiene care13 ; therefore, many surgeons who perform implant surgery try to ensure that there is sufficient keratinized attached mucosa around the implant. Nonetheless, sometimes this comes as a challenge, especially in the mandibular molar area due to lack of keratinized mucosa and collapse of attached mucosa after tooth extraction. Additional mucogingival surgery, such as the free gingival graft (FGG), helps in improving the thickness of attached gingiva but is known as a highly sensitive procedure.14,15  The worst complication following FGG is bleeding from the greater palatal artery, which emerges from the greater palatine foramen and runs anteriorly.16  Several clinical studies have demonstrated a safe zone for FGG that is away from the greater palatal artery, but the anatomy of the greater palatal artery may vary markedly among patients. The ability to detect the exact location of greater palatal artery would make FGG a more feasible and safer procedure, not only for the dentist but also for the patients in terms of minimizing the probability of excessive bleeding.

In this case report, we describe a case of an FGG used to regain attached gingiva around a dental implant in which a specially designed intraoral ultrasound probe was employed for localizing the greater palatal artery.

Technical Report

A 36-year-old female patient presented with complaints of gingival swelling, pain, and a mobile left mandibular second molar. After performing physical and radiographic evaluations, the tooth was diagnosed with horizontal root fracture and periodontitis. Treatment options for restoring the lower second molar were explained to the patient, and the patient agreed to tooth extraction and implant placement. Tooth extraction was performed without surgical intervention on the alveolar bone, but a considerable amount of inflammatory tissue was present around the tooth. The healing of the alveolar socket was uneventful, showing both insufficient bone and soft tissue. Six months after the extraction, implant placement surgery was performed with an alveolar bone graft, using a Superline implant (6.0 mm × 10 mm; Dentium, Seoul, Korea) and Bio-Oss (Geistlich Pharma, Wolhusen, Switzerland). Treatment was delayed due to maternity leave, and the second implant surgery was conducted 2 years after the dental implant placement. An apically positioned flap technique was used (healing abutment size: 6.5 mm in diameter and short height). Because a considerable amount of keratinized gingiva was lost after extraction, even an apically positioned flap was unable to preserve the attached keratinized mucosa buccal of healing abutment (Figures 1 and 2). Therefore, a free keratinized gingival graft was planned that could obtain attached keratinized free gingiva.

Figures 1–5

Figure 1. Preoperative clinical finding showing a lack of attached gingiva around the healing abutment. Figure 2. Preoperative periapical X ray showing that the implant for the second molar was placed and maintained well. Figure 3. US imaging device and intraoral probe. Figure 4. Insertion of the oral probe for detecting the great palatine artery and measuring the thickness of the palatal gingiva. Figure 5. Ultrasound Doppler image of the palatal mucosa showing the course of the greater palatal artery and the thickness of the palatal gingiva (blue line: outline of palatal gingiva, red dot: great palatal artery, green line: palate).

Figures 1–5

Figure 1. Preoperative clinical finding showing a lack of attached gingiva around the healing abutment. Figure 2. Preoperative periapical X ray showing that the implant for the second molar was placed and maintained well. Figure 3. US imaging device and intraoral probe. Figure 4. Insertion of the oral probe for detecting the great palatine artery and measuring the thickness of the palatal gingiva. Figure 5. Ultrasound Doppler image of the palatal mucosa showing the course of the greater palatal artery and the thickness of the palatal gingiva (blue line: outline of palatal gingiva, red dot: great palatal artery, green line: palate).

We planned to harvest FGG from the maxillary palate due to the thickness of the keratinized mucosa, good accessibility, and high quality of gingiva. The greater palatine artery and greater palatine nerves (originating from the greater palatine foramen) are known to be anatomic structures at risk during gingiva harvesting from this area. Therefore, to avoid possible damage to the greater palatine artery, a specially designed intraoral ultrasound probe was used to safely localize the greater palatal artery.

The palate from the greater palatine foramen to the ipsilateral canine tooth was observed using a transducer that could operate at 3∼12 MHz and was specially designed to deploy inside the mouth installed on a US imaging device (E-cube 9, Alpinion, Seoul, Korea) with an intraoral ultrasonic probe (IO8-17, Alpinion; Figures 3 and 4). The bloodstream was observed by operating the device in Doppler imaging mode (Figure 5). The greater palatine artery could be easily located since it exhibited marked pulsation in Doppler mode, and the flow inside the artery was determined. The search did not reveal any specific collateral branches.

The donor site and the recipient site (the buccal side of the healing abutment for implant in the left mandibular second molar) were then minimally anesthetized (2% lidocaine, 1:100 000 epinephrine) to prevent inactivation and delayed healing of either the donor or recipient site due to epinephrine's suppression of blood flow. A partial gingival flap was first formed at the recipient site and lifted, and then part of the top area was resected and placed in an apically positioned flap operation.

A safety zone that avoided the revealed course of the greater palatine artery while allowing harvesting of free gingiva was determined (Figure 6). A sufficient size of free gingiva (10 mm × 5 mm) was harvested in this zone by complete separation from the alveolar periosteum. A small amount of bleeding occurred at the donor site, but no arterial bleeding or massive hemorrhage was present. The harvested free gingiva was kept in saline solution and pressure hemostasis was ensured at the donor site using a collagen matrix (Bio-gide, Geistlich Pharma) and a palatal wafer. The harvested keratinized free gingiva was then placed adjacent to the side of the healing abutment for the implant without any dead space and sutured to the alveolar periosteum (Figure 7).

Figures 6 and 7

Figure 6. Harvesting palatal gingiva while the great palatal artery is preserved. Figure 7. Comparison of pre- and postoperative views. A sufficient amount of free gingival graft could be placed around the healing abutment.

Figures 6 and 7

Figure 6. Harvesting palatal gingiva while the great palatal artery is preserved. Figure 7. Comparison of pre- and postoperative views. A sufficient amount of free gingival graft could be placed around the healing abutment.

Discussion

The conventional FGG has been typically applied to open exposed root surfaces resulting from gingival recession.1417  This procedure has also been performed to improve the form of the marginal gingiva in areas with esthetic importance, such as the anterior tooth area, or to expand keratinized gingiva areas for supporting the bottom of a removable denture. The increasing popularity of dental implant treatment has recently led to the widespread use of FGGs to improve plaque control and gingival sealing supported by keratinized gingiva around the prosthetic crown of an implant.18  Studies have shown that keratinized gingiva around implant prostheses does not significantly contribute to plaque control nor prevention of germ invasion. However, clinical experience has led to dentists preferring application of keratinized gingiva to the area surrounding a dental implant.13,18 

Because the posterior mandible shows narrow keratinized gingiva, it is difficult to surround implant prostheses with keratinized gingiva. The following methods are commonly used to resolve this situation: First, during the second surgery, the attached gingiva of the superior alveolar bone crest is placed on the inferior site by an apically positioned flap, or the keratinized gingiva is widened using an FGG.17  Second, thick membrane-shaped mucosal graft material made from porcine collagen or other substitutes is used. Although positioning an apical flap is a simple procedure, its usefulness is limited when there is insufficient keratinized gingiva. Various mucosal graft materials have been released in the market, but careful attention is necessary to avoid unsuccessful engraftment or contamination. The main shortcoming of the FGG is that the additional wound leads to pain, extra bleeding, and the likelihood of infection at the exposed donor site.

The donor sites of keratinized gingiva include the maxillary palate, maxillary tuberosity, and mandibular retromolar area. The maxillary palate is often considered as the first choice because it is possible to harvest a thick graft from the plentiful keratinized gingiva existing in the area. However, the greater palatine artery and greater palatine nerves—originating from the greater palatine foramen and running anteriorly—are known to be anatomic structures at risk during gingiva harvesting.16  A high rate of absorption is observed for free keratinized gingival grafts, and this may impair the prognosis. For these reasons, it is recommended to graft 30–60% more keratinized gingiva than is thought to be needed. This implies that a large graft needs to be harvested, which can result in damage or bleeding of the artery if not detected clearly.

Previous reports have provided anatomic information for avoiding the greater palatine artery and greater palatine nerves. Sebastian et al16  studied 41 cadavers and reported that the height from the gum ridge to the palatal vault was 5.7 ± 2.2 mm in the first premolar region and 7.9 ± 2.1 mm in the second molar region. However, these statistics reflect the presence of huge individual variations, including variations due to sex and skeleton size. Further, the possible presence of branches from the premolar and molar regions increase the risks of arterial bleeding. Thus, to prevent unexpected arterial damage and bleeding, it is critical to determine the course of the artery in each patient.

In the present case, the course of the artery was directly evaluated using a hockey-stick, linear-array, intraoral ultrasonic probe that was developed for dental applications. Because operation in Doppler mode reveals fluid flow in the bloodstream, color coding can be used to distinguish arteries and veins. In addition, by using a pulsating flow, arteries can be observed accurately since real-time imaging is possible. However, administering an anesthetic agent containing epinephrine leads to vessel constriction; therefore, the arterial measurement should be performed before anesthesia.

The flap was planned in the present patient while avoiding the course of the artery that had been measured on the same side (left) of the palate, and a 5 mm × 10 mm graft was harvested successfully. The outcome of the free keratinized gingival graft depends crucially on the acceptance of FGG at the recipient site. Prompt treatment and suturing without dead space are critical; thus, the result is highly dependent on the operator's skills. The graft thickness is also important, as well as the size of the contacting donor and recipient site (sutured area) when fixing the flap. If the graft is too thick for the recipient site, it is not possible to achieve coverage and an adequate blood supply. Conversely, if it is too thin for the site, absorption or necrosis can occur, or the area could be torn during harvesting and suturing.19 

When the graft is harvested from the donor site, the inclusion of connective tissue and periosteum are determined by the thickness of the flap at the donor and recipient sites. The recommended measurement method for the palatal flap thickness is using a dental probe before surgery. However, this may be restricted by possible severe pain. Panoramic radiographs do not show much information about the gingiva. Although Song et al reported the thickness of the plate gingiva (3.83 ± 0.58 mm) based on CT, this information needs to be determined on a case-by-case basis due to the following characteristics: Gingiva is thicker in males than in females, gingiva thickens with age, and a plate gingiva flap is thicker in the premolar region than in the molar and canine regions.20,21  A noninvasive method, US makes it possible to measure the gingiva thickness at multiple points and at different angles, which is helpful for selecting the most appropriate donor site based on the gingiva at the recipient site.

The use of US is not new in dentistry,22  but its applications in oral surgery and oral medicine have been limited.23,24  Other researchers reported US to be useful in diagnosing Warthin's tumor in the internal parotid gland.25,26  Bialec et al27  reported that US can be helpful in the differential diagnosis of a swelling or tumor inside the large salivary glands. Nisha et al28  recently reported the effectiveness of color Doppler US for assessing the spatial extent of an infection on the face. Ariji et al6,8,29  reported that US was useful for the diagnosis and treatment assessment in the masseter and the temporomandibular joint.

The limitation of our study is that it is a single case report covering one FGG case. To strengthen our findings, a case series of patients is recommended. Further clinical studies such as case series or prospective cohort studies measuring quantitative data (eg, tissue thickness, size of the area, and safe area for donor sites) should be followed to verify this innovative tool. Soft tissue harvesting procedures other than FGG, such as connective tissue graft, can be aided by the non-ionizing, ultrasound probe for safer, more accurate surgery. These clinical trials may be beneficial not only for the dentist but also for patients in terms of safe and predictable results of mucogingival surgical procedures.

Abbreviations

    Abbreviations
     
  • 3D

    three-dimensional

  •  
  • CBCT

    cone-beam computed tomograph

  •  
  • CT

    computed tomography

  •  
  • FGG

    free gingival graft

  •  
  • MRI

    magnetic resonance imaging

  •  
  • US

    ultrasonography

Note

Kee-Deog Kim has a grant supported by Alpinion Co for testing probe and academic consultation. The other authors have no conflicts of interest in this study.

References

References
1
American Dental Association Council on Scientific A
.
The use of cone-beam computed tomography in dentistry: an advisory statement from the American Dental Association Council on Scientific Affairs
.
J Am Dent Assoc
.
2012
;
143
:
899
902
.
2
Spin-Neto
R,
Stavropoulos
A,
Dias Pereira
LA,
Marcantonio
E
Jr,
Wenzel
A.
Fate of autologous and fresh-frozen allogeneic block bone grafts used for ridge augmentation. A CBCT-based analysis
.
Clin Oral Implants Res
.
2013
;
24
:
167
173
.
3
Becker
A,
Chaushu
S,
Casap-Caspi
N.
Cone-beam computed tomography and the orthosurgical management of impacted teeth
.
J Am Dent Assoc
.
2010
;
141
(
suppl 3
):
14S
18S
.
4
Berris
T,
Gupta
R,
Rehani
MM.
Radiation dose from cone-beam CT in neuroradiology applications
.
AJR Am J Roentgenol
.
2013
;
200
:
755
761
.
5
Kim
S,
Yoshizumi
TT,
Frush
DP,
Toncheva
G,
Yin
FF.
Radiation dose from cone beam CT in a pediatric phantom: risk estimation of cancer incidence
.
AJR Am J Roentgenol
.
2010
;
194
:
186
190
.
6
Ariji
Y,
Kimura
Y,
Gotoh
M,
Sakuma
S,
Zhao
YP,
Ariji
E.
Blood flow in and around the masseter muscle: normal and pathologic features demonstrated by color Doppler sonography
.
Oral Surg Oral Med Oral Pathol Oral Radiol Endod
.
2001
;
91
:
472
482
.
7
Ariji
Y,
Nakayama
M,
Nishiyama
W,
Nozawa
M,
Ariji
E.
Shear-wave sonoelastography for assessing masseter muscle hardness in comparison with strain sonoelastography: study with phantoms and healthy volunteers
.
Dentomaxillofac Radiol
.
2016
;
45
:
20150251
.
8
Ariji
Y,
Nakayama
M,
Nishiyama
W,
et al.
Can sonographic features be efficacy predictors of robotic massage treatment for masseter and temporal muscle in patients with temporomandibular disorder with myofascial pain?
Cranio
.
2016
;
34
:
13
19
.
9
Ariji
Y,
Kimura
Y,
Hayashi
N,
et al.
Power Doppler sonography of cervical lymph nodes in patients with head and neck cancer
.
AJNR Am J Neuroradiol
.
1998
;
19
:
303
307
.
10
Hayashi
T,
Ito
J,
Koyama
J,
Yamada
K.
The accuracy of sonography for evaluation of internal derangement of the temporomandibular joint in asymptomatic elementary school children: comparison with MR and CT
.
AJNR Am J Neuroradiol
.
2001
;
22
:
728
734
.
11
Li
C,
Su
N,
Yang
X,
Yang
X,
Shi
Z,
Li
L.
Ultrasonography for detection of disc displacement of temporomandibular joint: a systematic review and meta-analysis
.
J Oral Maxillofac Surg
.
2012
;
70
:
1300
1309
.
12
Ariji
Y,
Yuasa
H,
Ariji
E.
High-frequency color Doppler sonography of the submandibular gland: relationship between salivary secretion and blood flow
.
Oral Surg Oral Med Oral Pathol Oral Radiol Endod
.
1998
;
86
:
476
481
.
13
Greenstein
G,
Cavallaro
J.
The clinical significance of keratinized gingiva around dental implants
.
Compend Contin Educ Dent
.
2011
;
32
:
24
31
;
quiz 32, 34
.
14
Miller
PD
Jr.
Root coverage with the free gingival graft. Factors associated with incomplete coverage
.
J Periodontol
.
1987
;
58
:
674
681
.
15
Paolantonio
M,
di Murro
C,
Cattabriga
A,
Cattabriga
M.
Subpedicle connective tissue graft versus free gingival graft in the coverage of exposed root surfaces. A 5-year clinical study
.
J Clin Periodontol
.
1997
;
24
:
51
56
.
16
Klosek
SK,
Rungruang
T.
Anatomical study of the greater palatine artery and related structures of the palatal vault: considerations for palate as the subepithelial connective tissue graft donor site
.
Surg Radiol Anat
.
2009
;
31
:
245
250
.
17
de Sanctis
M,
Clementini
M.
Flap approaches in plastic periodontal and implant surgery: critical elements in design and execution
.
J Clin Periodontol
.
2014
;
41
(
suppl 15
):
S108
122
.
18
Simons
AM,
Darany
DG,
Giordano
JR.
The use of free gingival grafts in the treatment of peri-implant soft tissue complications: clinical report
.
Implant Dent
.
1993
;
2
:
27
30
.
19
Hwang
D,
Wang
HL.
Flap thickness as a predictor of root coverage: a systematic review
.
J Periodontol
.
2006
;
77
:
1625
1634
.
20
Cha
BK,
Lee
YH,
Lee
NK,
Choi
DS,
Baek
SH.
Soft tissue thickness for placement of an orthodontic miniscrew using an ultrasonic device
.
Angle Orthod
.
2008
;
78
:
403
408
.
21
Song
JE,
Um
YJ,
Kim
CS,
et al.
Thickness of posterior palatal masticatory mucosa: the use of computerized tomography
.
J Periodontol
.
2008
;
79
:
406
412
.
22
Baum
G,
Greenwood
I,
Slawski
S,
Smirnow
R.
Observation of internal structures of teeth by ultrasonography
.
Science
.
1963
;
139
:
495
496
.
23
Ghorayeb
SR,
Bertoncini
CA,
Hinders
MK.
Ultrasonography in dentistry
.
IEEE Trans Ultrason Ferroelectr Freq Control
.
2008
;
55
:
1256
1266
.
24
Marotti
J,
Heger
S,
Tinschert
J,
et al.
Recent advances of ultrasound imaging in dentistry – a review of the literature
.
Oral Surg Oral Med Oral Pathol Oral Radiol
.
2013
;
115
:
819
832
.
25
Kim
J,
Kim
EK,
Park
CS,
Choi
YS,
Kim
YH,
Choi
EC.
Characteristic sonographic findings of Warthin's tumor in the parotid gland
.
J Clin Ultrasound
.
2004
;
32
:
78
81
.
26
Rong
X,
Zhu
Q,
Ji
H,
Li
J,
Huang
H.
Differentiation of pleomorphic adenoma and Warthin's tumor of the parotid gland: ultrasonographic features
.
Acta Radiol
.
2014
;
55
:
1203
1209
.
27
Zajkowski
P,
Jakubowski
W,
Bialek
EJ,
Wysocki
M,
Osmolski
A,
Serafin-Krol
M.
Pleomorphic adenoma and adenolymphoma in ultrasonography
.
Eur J Ultrasound
.
2000
;
12
:
23
29
.
28
Aarthi Nisha
V,
Parthiban
J,
Santana
N,
et al.
The role of colour Doppler ultrasonography in the diagnosis of fascial space infections – a cross sectional study
.
J Clin Diagn Res
.
2013
;
7
:
962
967
.
29
Ariji
Y,
Katsumata
A,
Hiraiwa
Y,
et al.
Masseter muscle sonographic features as indices for evaluating efficacy of massage treatment
.
Oral Surg Oral Med Oral Pathol Oral Radiol Endod
.
2010
;
110
:
517
526
.

Author notes

These authors contributed equally to this work.