This case report seeks to describe efficient clinical application of adipose-derived stem cells (AdSCs) originated from buccal fat pad (BFP) in combination with conventional guided bone regeneration as protected healing space for reconstruction of large alveolar defects after extraction of multiple impacted teeth. The first case was a 19-year-old woman with several impacted teeth in the maxillary and mandibular regions, which could not be forced to erupt and were recommended for surgical extraction by the orthodontist. After this procedure, a large bone defect was created, and this space was filled by AdSC loaded natural bovine bone mineral (NBBM), which was protected with lateral ramus cortical plates, microscrews, and collagen membrane. After 6 months of post-guided bone regeneration, the patient received 6 and 7 implant placements, respectively, in the maxilla and mandible. At 10 months postoperatively, radiographic evaluation revealed thorough survival of implants. The second case was a 22-year-old man with the same complaint and large bony defects created after his teeth were extracted. After 6 months of post-guided bone regeneration, he received 4 dental implants in his maxilla and 7 implants in the mandible. At 48 months postoperatively, radiographs showed complete survival of implants. This approach represented a considerable amount of 3-dimensional bone formation in both cases, which enabled us to use dental implant therapy for rehabilitation of the whole dentition. The application of AdSCs isolated from BFP in combination with NBBM can be considered an efficient treatment for bone regeneration in large alveolar bone defects.

Bone regenerative therapies, especially stem cell–based treatment, requires a consistent source of osteoprogenitor cells.1  Although bone marrow aspirates reveal the most well-known origin of stem cells for bone tissue engineering,25  the invasive procedure for harvesting the tissue and decreasing osteogenic capability of bone marrow mesenchymal stem cells (BMMSCs) after a certain age1,6  challenge its beneficial application. Thus, a multitude of alternative sources, including dental tissues,710  skeletal muscle,11  and adipose tissue,1214  have been proposed. Among these recent sources, adipose-derived stem cells (AdSCs) were successfully used in several in vitro,1517  in vivo,1820  and clinical investigations2123  for bone repair. In comparison to BMMSCs, AdSCs revealed longer conservation in culture and maintained their proliferation and osteogenic differentiation capabilities.24  Moreover, these multipotent cells in adipose tissues are easily accessible. Also, their harvesting procedure is less invasive, and they are abundant in the human body.1,24  Buccal fat pad (BFP) is a specialized form of subcutaneous rich vascularized fatty tissue in the oral cavity,25  which has been investigated as an attractive graft for bone and periodontal repair in oral surgery.2629  Furthermore, BFP has been shown to be a valuable source of AdSCs, capable of differentiating into osteoblast.30 

In order to reconstruct large bone defects in the craniofacial region, which are caused by congenital factors, trauma, and various pathologies,31  a cell-based approach can be beneficial in overcoming some drawbacks of conventional methods, such as obtaining iliac crest autograft, which causes a considerable morbidity in the donor site.3235  In this regard, application of AdSCs originated from BFP, that is, BFP-derived stem cells (BFPSCs) can simplify surgical procedures and diminish clinical risks compared with large autograft harvesting.36  However, based on our investigation, no published articles have assessed stem cells derived from BFP for large craniofacial rehabilitations. This case report sought to evaluate and describe the potential clinical application of AdSCs originated from BFP in combination with conventional guided bone regeneration (GBR) as protected healing space for reconstruction of large alveolar defects after extraction of multiple teeth extractions.

In the current study, 2 patients presenting to the Department of Oral Maxillofacial Surgery, Shahid Beheshti University of Medical Sciences, were identified. The clinical procedures were confirmed by the Ethics Committee of Shahid Behesti University of Medical Sciences. The patients gave informed consent for BFP harvesting and surgical procedures.

BFPSC isolation and cultivation

Three weeks before graft surgery, patients' BFPs were exposed through a vestibular incision in the posterior part of the mandible as previously described.37  Next, 3–5 mL of adipose tissue was excised and sent to the laboratory. The obtained adipose tissues were placed in a solution of 1% collagenase type I (Sigma-Aldrich, St Louis, Mo) for 1 hour at 37°C in an incubator shaker. Then, cells were resuspended in growth medium containing Dulbecco Modified Eagle Medium (Life Technologies, Carlsbad, Calif) and 10% autogenous human serum. Cell suspension was transferred to a T-25 flask and incubated at 37°C and 5% CO2. Cells were cultured after 80% to 90% confluency. The medium was changed every 3 days. Cells were trypsinized using 0.25% trypsin-ethylenediaminetetraacetic acid (Life Technologies).38 

BFPSC characterization

Flow Cytometry Analysis

In order to characterize the human AdSCs, cell surface expression of CD90, CD44, CD73, CD105, CD34, and CD45 was measured by fluorescence absorbance cell sorting analysis using standard protocols. For the flow cytometry process, phycoerythrin (PE)–conjugated monoclonal antibodies and fluorescent isothiocyanate (FITC)–conjugated monoclonal antibodies were used according to the specific device (BD FACSCalibur; BD Biosciences, Franklin Lakes, NJ). Then, anti-CD44-FITC, anti-CD73-PE, anti-CD90-FITC, anti-CD45-FITC, anti-CD105-PE, and anti-CD34-PE (EXBIO Praha, Vestec, Czech Republic) were applied at 2 mg/mL. Stem cells dyed with FITC-labeled mouse immunoglobulin G were used as a negative control. After washing with phosphate-buffered saline, all specimens were fixed using 1% paraformaldehyde. Flow cytometry data were analyzed using FlowJo 7.6.1 software (FlowJo LLC, Ashland, Ore); samples with >90% fluorescent-labeled cells were considered positive.

Cell Differentiation Analysis

The BFPSCs were also assessed for osteogenic differentiation. Cells at passage 3 were placed in Stem PRO (Life Technologies) for 14 days and then fixed using paraformaldehyde solution. Next, they were stained with Alizarin red for 5 minutes and imaged using light microscopy.

Stem-cell seeding

In this study, natural bovine bone mineral (NBBM) (1521, Cerabone granules, Botiss, Berlin, Germany) with a crystalline size of 1.0–2.0 mm, which mimics the same characteristic of the human normal bone, was used.39  Five mg of NBBM was placed into 96-well plates, and BFPSCs at density of 105 cells per well were seeded on them for 48 hours at 37°C and 5% CO2.

Scanning electron microscopy

The attachment of BFPSCs on NBBM was examined using scanning electron microscopy (SEM), and the cells on the scaffolds were fixed by 2.5% glutaraldehyde for 1 hour at room temperature. Dehydration cell scaffold was done in a series of increasing concentrations of ethanol in distilled water 30%, 70%, 80%, 90%, and 100% for 10 minutes per each concentration. The samples were air-dried for 24 hours. Finally, the scaffolds were sputter-coated with gold before imaging (SU3500, Hitachi, Tokyo, Japan).

Case 1

In September 2015, a 19-year-old woman was referred to the clinic complaining of several impacted teeth in the maxillary and mandibular regions, which could not be forced to erupt and were recommended for surgical extraction by the orthodontist. The patient has cleidocranial dysplasia. She was a nonsmoker with no systemic health problem (aortic stenosis and aortic insufficiency [ASAI]). Preoperative radiographic assessment revealed 11 impacted teeth in the upper jaw and 13 in the lower jaw between the first molars (Figure 1). All teeth were removed after being exposed through the buccal bone with minimum bone removal. In deeply impacted teeth, thin labial bone was cut with a Piezosurgery saw blade (Mectron, Carasco, Italy) and out fractured to expose the teeth. A protected healing space was created by fixing the out-fractured bone or by using the adjacent lateral ramus cortical bone stabilized with a microplate (1.2 mm, Jeil, Seoul, South Korea). Then, NBBM (1521, Cerabone granules, Botiss) coated with BFPSCs was delivered and filled the space. After 6 months post-GBR, she underwent 6 and 7 dental implant (Alfit, SSO, IDHE Dental Implant Company, Bern, Switzerland) placements, respectively, in the maxilla and mandible. At 10 months postoperatively, panoramic radiographic evaluations revealed thorough survival of implants.

Figure 1

Preoperative radiographs of patient 1 showing multiple impacted teeth; note the impacted teeth in the mandible and maxilla. (a) Panoramic view. Cone-beam computerized tomography evaluations of (b) maxilla at coronal plane and (c) sagittal plane.

Figure 1

Preoperative radiographs of patient 1 showing multiple impacted teeth; note the impacted teeth in the mandible and maxilla. (a) Panoramic view. Cone-beam computerized tomography evaluations of (b) maxilla at coronal plane and (c) sagittal plane.

Case 2

In December 2012, a 22-year-old man was referred to the clinic, complaining of several impacted teeth in the maxillary and mandibular regions, which had not achieved erupted, and the orthodontist suggested surgical extraction. This patient was non-smoker with no systemic condition (ASAI). Preoperative radiographic assessment showed 12 impacted teeth in the upper jaw and 10 in the lower jaw between the first molars (Figure 2). At 12 months post-GBR, he received 4 dental implants (Alfit, SSO, IDHE Dental Implant Company) in his maxilla and 7 dental implants (Alfit, SSO, IDHE Dental Implant Company) in the mandible. At 48 months postoperatively, panoramic radiographic evaluations revealed thorough survival of implants.

Figure 2

Preoperative radiographs of patient 2 showing multiple impacted teeth. (a) Panoramic view. Cone-beam computerized tomography evaluations at coronal plane and sagittal plane of (b) maxilla and (c) mandible.

Figure 2

Preoperative radiographs of patient 2 showing multiple impacted teeth. (a) Panoramic view. Cone-beam computerized tomography evaluations at coronal plane and sagittal plane of (b) maxilla and (c) mandible.

Surgical method

A crestal incision was made molar to molar in the mandible and maxilla, with 2 releasing incisions. Subperiosteal dissection of the buccal and lingual mucosal flaps was performed gently. The impacted teeth were exposed with the delicate removal of the buccal plate after use of the Piezosurgery microsaw. In some places, superficially located teeth lead to out-fracture of thin covering bone. After extraction of impacted teeth, an extra-large (>6 cm) bone defect was created in the maxilla and mandible. A cortical autogenous bone block was harvested from the l00ateral ramus of the mandible on both sides. The obtained bone tissue was cut into 3 or 4 pieces. The thin labia plate and 1.2-mm microscrews with lateral ramus cortical plates were fixed together to create a protected healing space (Figures 3a and 4a). The space was filled with NBBM loaded with BFPSCs (Figures 3b and 4b). The whole construct was covered with collagen membrane (Jason Membrane, Botiss) and sutured (5/0 polyglactin 910, Vicryl, Ethicon, Sint-Stevens-Woluwe, Belgium) (Figures 3c and 4c). Subsequently, the retracted flap was replaced to its position and closed by continuous horizontal mattress sutures. All procedures were done in a hospital setting by an experienced oral and maxillofacial surgeon and his team.

Figures 3–5

Figure 3. Intraoperative image of patient 1. (a) Fixation of lateral ramus cortical bone via microscrew and plates, defect site was filled by (b) stem cell loaded scaffold and (c) collagen membrane placement in order to preserve the healing space and sutured. Figure 4. Intraoperative image of patient 2. (a) Fixation of lateral ramus cortical bone via microscrew and plates. Defect site was filled by (b) stem cell loaded scaffold and (c) collagen membrane placement in order to preserve the healing space and covering the graft. Figure 5. Intraoperative image of patient 2. (a) Clinical view of regenerated bone after flap repositioning, (b) Dental implant placements at 7 months postoperatively.

Figures 3–5

Figure 3. Intraoperative image of patient 1. (a) Fixation of lateral ramus cortical bone via microscrew and plates, defect site was filled by (b) stem cell loaded scaffold and (c) collagen membrane placement in order to preserve the healing space and sutured. Figure 4. Intraoperative image of patient 2. (a) Fixation of lateral ramus cortical bone via microscrew and plates. Defect site was filled by (b) stem cell loaded scaffold and (c) collagen membrane placement in order to preserve the healing space and covering the graft. Figure 5. Intraoperative image of patient 2. (a) Clinical view of regenerated bone after flap repositioning, (b) Dental implant placements at 7 months postoperatively.

Patients were all given 500 mg amoxicillin 3 times a day for a week, analgesics (ibuprofen 400 mg with or without acetaminophen codeine 300/10 mg depending on the severity of the pain), and 1 intramuscular injection of 8 mg dexamethasone (Alborz Darou, Tehran, Iran) and chlorhexidine mouthwash 0.2% (Behsa Pharmaceutical, Tehran, Iran) for 7 days postoperatively. In the consolidation period before implant therapy (4–6 months after surgery), patients were visited twice a week for the first month and monthly prior to dental implant placement. Figure 5 shows the clinical view of the new bone formation in case 1 before and after implant installation.

Clinical assessment

In order to evaluate clinical healing, soft tissue and the healing process of grafted tissue were checked biweekly for the first month postoperatively and then monthly for 6 months.

Radiographic analysis

Patients had 2 cone beam computed tomography scans taken on the NewTom VG 9000 device (Quantitative Radiology SRL Co, Verona, Italy) before and 6 months after graft surgery. Panoramic view radiographs were taken in the follow-up periods after dental implant placement. A calibrated oral and maxillofacial surgeon qualitatively evaluated the amount of bone.

Histologic evaluation

Trephine samples were obtained during implant installation. All specimens were fixed in 10% buffered-formalin for 5 to 7 days, and decalcified in formic acid and sodium citrate for 24 hours. The specimens were washed with tap water, dehydrated with ascending concentrations of ethyl alcohol, cleared in xylene (Sigma-Aldrich), and infiltrated with paraffin. Serial sections (5 μm) parallel to the midsagittal suture were cut from the center of each specimen using a microtome and stained with hematoxylin and eosin.

The sections were viewed and qualitatively analyzed for new bone formation, residual bone substitute, residual clot elements, soft tissue elements, and inflammatory reactions by 1 calibrated examiner using polarized light microscopy (SZX 9, Olympus, Tokyo, Japan).

In vitro findings

Flow Cytometry

Flow cytometric analysis of harvested and cultured BFPSCs indicated that more than 95 of the cells were positive for mesenchymal markers (CD73 , CD105, CD 44, and CD 90). Hematopoietic markers (CD34 and CD45) were expressed at very low percentages of the cells (Figure 6).

Figure 6

Flow cytometry analysis of harvested and cultured buccal fat pad stem cells; 95% of cells were positive for mesenchymal markers (CD73 [SH3] and CD105 [SH2]) and cell adhesion molecules (CD 44 and CD 90). Hematopoietic markers (CD34 and CD45) were expressed at very low percentages of the cells.

Figure 6

Flow cytometry analysis of harvested and cultured buccal fat pad stem cells; 95% of cells were positive for mesenchymal markers (CD73 [SH3] and CD105 [SH2]) and cell adhesion molecules (CD 44 and CD 90). Hematopoietic markers (CD34 and CD45) were expressed at very low percentages of the cells.

Alizarin Red Staining

Alizarin red staining findings represented deposition of mineralized nodule-like structures and confirmed the osteogenic capability of the cultured cells (Figure 7).

Figures 7–9

Figure 7. Alizarin red staining (×40); mineralized nodule-like structures represent osteogenic differentiation of stem cells. Figure 8. Scanning electron microscope view of buccal fat pad derived stem cells' attachment to natural bovine bone mineral scaffold. Figure 9. Postoperative radiographs of patient 1 showed the considerable amount of new bone formation in the (a) maxilla and (b) and mandible 6 months postoperatively.

Figures 7–9

Figure 7. Alizarin red staining (×40); mineralized nodule-like structures represent osteogenic differentiation of stem cells. Figure 8. Scanning electron microscope view of buccal fat pad derived stem cells' attachment to natural bovine bone mineral scaffold. Figure 9. Postoperative radiographs of patient 1 showed the considerable amount of new bone formation in the (a) maxilla and (b) and mandible 6 months postoperatively.

SEM

Figure 8 presents the SEM image of BFPSCs in 3-dimensional scaffold culture after 48 hours. Stem cells demonstrated a similar spindle-shaped morphology and attachment to the NBBM.

In vivo findings

All through the study, the patients' healing processes were uneventful, and there were no serious complication. In case 1, as seen in Figure 9, after 7 months radiographic assessment revealed the proper amount of newly regenerated bone in the upper and lower jaws (Figure 5). Radiographic evaluations revealed acceptable integration of bone substitute to the recipient healthy bone and 3-dimensional bone formation. In addition, clinical observation indicated a bony dense and vascularized tissue after dislocation of surgical flap. Figure 10a shows osseointegrated implants after 10 months.

Figures 10–12

Figure 10. Panoramic radiographs of dental implant placement: (a) patient 1 after 10 months and (b) patient 2 at 48 months postoperatively. Figure 11. Postoperative radiographs of patient 2 showing the significant amount of bone regeneration in the (a) maxilla and (b) mandible 6 months postoperatively. Figure 12. The trabecular pattern was mostly lamellar organization, containing osteocytes within lacunae and (a) a fibrous bone marrow (hematoxylin and eosin [H&E], ×40), osteocytes (white arrows), osteoblastic rim (black arrow), and residual body (Asterix) are shown in the histogram B (H&E, ×40).

Figures 10–12

Figure 10. Panoramic radiographs of dental implant placement: (a) patient 1 after 10 months and (b) patient 2 at 48 months postoperatively. Figure 11. Postoperative radiographs of patient 2 showing the significant amount of bone regeneration in the (a) maxilla and (b) mandible 6 months postoperatively. Figure 12. The trabecular pattern was mostly lamellar organization, containing osteocytes within lacunae and (a) a fibrous bone marrow (hematoxylin and eosin [H&E], ×40), osteocytes (white arrows), osteoblastic rim (black arrow), and residual body (Asterix) are shown in the histogram B (H&E, ×40).

In case 2, radiographic assessment showed appropriate amount of bone both in height and width for implant therapy after 12 months (Figure 11). Overall, the regenerated bone in case 2 was similar to that of the previous patient and depicted a bony hard clinical appearance and high vascularity during the specimen harvesting and implant placement process. Figure 10b shows osseointegrated implants after 48 months.

In both cases, new bone and osteoid matrix formation with incorporation into the NBBM were seen (Figure 12a and b). The trabecular pattern was mostly lamellar organization containing osteocytes within lacunae and rimmed via osteoblasts. There was no evidence of foreign body reaction, and there was considerable immune response in the obtained specimens from both patients.

Autogenous iliac crest bone graft is the gold standard for rehabilitation of large bone defects40  due to its rapid incorporation to the host, the presence of a multitude of growth factors, and its osteogenic properties.41  However, there are some major drawbacks in its clinical application, such as the need for a second site of surgery, its limited tissue volume, morbidity of donor site, infection, and scar creation.4143  In addition, it is estimated that up to 80% of the osteocytes do not survive the transplantation process between the donor site and the surgical site, and they showed a resorption rate between 65% and 85%.4447  Moreover, from a biological perspective, the origin of iliac crest harvested bone is the mesoderm germinal layer, which generates bone by endochondral ossification process, whereas bone grafts that are obtained intraorally from the mandible turn into bone much faster because they generate bone by intraosseous bone formation.48  Thus, the emergence of regenerative medicine to address these shortcomings of iliac crest harvested bone is pivotal. One of the most imperative purposes of bone tissue engineering is to seek a reliable source of stem cells that provide a proper number of stem cells for clinical administration with minimal invasiveness and morbidity. Nowadays, BMMSCs are the most common source of osteoprogenitor cells in bone tissue engineering4,5  that are isolated from bone marrow aspirate. However, this invasive and painful process has only 0.001% to 0.1% of BMMSCs in the obtained cells compared with lipoaspirates, which contain 1% to 5% of ADCSs.49  Moreover, the comparative investigations revealed similar osteogenic differentiation of AdSCs and BMMSCs.5052  In the current study, we used BFP as the adipose tissue source. In contrast to subcutaneous adipose tissue, BFP is a specialized mass of fat that is easy to harvest in oral surgery and causes less morbidity and complications in donor site.36,53,54  Moreover, BFP size is approximately similar in various persons and does not depend on fat distribution and body weight.55  Hence, it can be a primary source of stem cells for therapeutic purposes.

In spite of the intensifying amount of evidences on AdSCs and their excellent potential for bone regeneration, most in vitro investigations and only limited clinical trials have evaluated the safety and efficacy of AdSC use in humans.21,36,5658  In accordance with our results, AdSCs showed beneficial effects on bone healing in anterior mandibular,56  maxillary,57  and cranial58  bony defects. This study evaluated the efficacy of BFP-derived mesenchymal stem cells for 3= dimensional bone regeneration in alveolar defects greater than 6 cm after extraction of multiple impacted teeth. The findings in these cases show that in large alveolar bone defects, application of BFPSCs with the GBR technique maintains appropriate bone regeneration for dental implant placement. One of our study's limitations is our evaluation methods. Although radiographic images cannot separate areas of new bone formation from bone substitutes, histologic assessments indicated a lamellar trabecular pattern containing osteocytes that represent a new bone formation area. Another limitation is that due to ethical considerations, we did not have any control to compare our findings.

With the limitation of our study, this efficacious clinical application of BFPSCs for regeneration of alveolar bone opens a window into this promising new field of research that requires further efforts, especially randomized controlled clinical trials and histomorphometric assessments to lead an evidence-based decision making.

Abbreviations

    Abbreviations
     
  • AdSC

    adipose-derived stem cell

  •  
  • ASAI

    aortic stenosis and aortic insufficiency

  •  
  • BMMSC

    bone marrow mesenchymal stem cell

  •  
  • BFP

    buccal fat pad

  •  
  • BFPSC

    buccal fat pad stem cell

  •  
  • FITC

    fluorescent isothiocyanate

  •  
  • GBR

    guided bone regeneration

  •  
  • NBBM

    natural bovine bone mineral

  •  
  • PE

    phycoerythrin

  •  
  • SEM

    scanning electron microscopy

The authors report no conflicts of interest.

1
Zomorodian
E,
Baghaban Eslaminejad M. Mesenchymal stem cells as a potent cell source for bone regeneration
.
Stem Cells Int
.
2012
;
2012
:
980353
.
2
Fisher
JN,
Peretti
GM,
Scotti
C.
Stem cells for bone regeneration: from cell-based therapies to decellularised engineered extracellular matrices
.
Stem Cells Int
.
2016
;
2016
:
9352598
.
3
Khojasteh
A,
Behnia
H,
Dashti
SG,
Stevens
M.
Current trends in mesenchymal stem cell application in bone augmentation: a review of the literature
.
J Oral Maxillofac Surg
.
2012
;
70
:
972
982
.
4
Hosseinpour
S,
Ahsaie
MG,
Rad
MR,
Taghi Baghani M, Motamedian SR, Khojasteh A. Application of selected scaffolds for bone tissue engineering: a systematic review
.
Oral Maxillofac Surg
.
2017
;
21
:
109
129
.
5
Motamedian
SR,
Hosseinpour
S,
Ahsaie
MG,
Khojasteh
A.
Smart scaffolds in bone tissue engineering: a systematic review of literature
.
World J Stem Cells
.
2015
;
7
:
657
.
6
Zhou
S,
Greenberger
JS,
Epperly
MW,
et al.
Age-related intrinsic changes in human bone-marrow-derived mesenchymal stem cells and their differentiation to osteoblasts
.
Aging Cell
.
2008
;
7
:
335
343
.
7
Morad
G,
Kheiri
L,
Khojasteh
A.
Dental pulp stem cells for in vivo bone regeneration: a systematic review of literature
.
Arch Oral Biol
.
2013
;
58
:
1818
1827
.
8
Pejcic
A,
Kojovic
D,
Mirkovic
D,
Minic
I.
Stem cells for periodontal regeneration
.
Balkan J Med Genet
.
2013
;
16
:
7
11
.
9
Rezai-Rad
M,
Bova
JF,
Orooji
M,
et al.
Evaluation of bone regeneration potential of dental follicle stem cells for treatment of craniofacial defects
.
Cytotherapy
.
2015
;
17
:
1572
1581
.
10
Khojasteh
A,
Nazeman
P,
Rad
MR.
Dental stem cells in oral, maxillofacial and craniofacial regeneration
.
In
:
Huang GT-J, Thesleff I, eds. Dental Stem Cells
.
Berlin, Germany
:
Springer International Publishing
;
2016
:
143
165
.
11
Bosch
P,
Musgrave
DS,
Lee
JY,
et al.
Osteoprogenitor cells within skeletal muscle
.
J Orthop Res
.
2000
;
18
:
933
944
.
12
Zuk
PA,
Zhu
M,
Mizuno
H,
et al.
Multilineage cells from human adipose tissue: implications for cell-based therapies
.
Tissue Eng
.
2001
;
7
:
211
228
.
13
Khojasteh
A,
Nazeman
P,
Rad
MR.
Dental stem cells in oral, maxillofacial and craniofacial
.
In
:
Şahin
F,
Doğan
A,
Demirci
S,
eds
.
Dental Stem Cells. Stem Cell Biology and Regenerative Medicine
.
Berlin, Germany
:
Springer;
2016
.
14
Salehi-Nik
N,
Rad
MR,
Kheiri
L,
Nazeman
P,
Nadjmi
N,
Khojasteh
A.
Buccal fat pad as a potential source of stem cells for bone regeneration: a literature review
.
Stem Cells Int
.
2017
;
2017
:
8354640
.
15
Kern
S,
Eichler
H,
Stoeve
J,
Klüter
H,
Bieback
K.
Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue
.
Stem Cells
.
2006
;
24
:
1294
1301
.
16
Im
G-I,
Shin
Y-W,
Lee
K-B.
Do adipose tissue-derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow-derived cells?
Osteoarthr Cartil
.
2005
;
13
:
845
853
.
17
Dmitrieva
RI,
Minullina
IR,
Bilibina
AA,
Tarasova
OV,
Anisimov
SV,
Zaritskey
AY.
Bone marrow- and subcutaneous adipose tissue-derived mesenchymal stem cells: differences and similarities
.
Cell Cycle
.
2012
;
11
:
377
383
.
18
Murata
D,
Tokunaga
S,
Tamura
T,
et al.
A preliminary study of osteochondral regeneration using a scaffold-free three-dimensional construct of porcine adipose tissue-derived mesenchymal stem cells
.
J Orthop Surg Res
.
2015
;
10
:
35
46
.
19
Hicok
KC,
Du Laney
TV,
Zhou
YS,
et al.
Human adipose-derived adult stem cells produce osteoid in vivo
.
Tissue Eng
.
2004
;
10
:
371
380
.
20
Justesen
J,
Pedersen
SB,
Stenderup
K,
Kassem
M.
Subcutaneous adipocytes can differentiate into bone-forming cells in vitro and in vivo
.
Tissue Eng
.
2004
;
10
:
381
391
.
21
Mesimäki
K,
Lindroos
B,
Törnwall
J,
et al.
Novel maxillary reconstruction with ectopic bone formation by GMP adipose stem cells
.
Int J Oral Maxillofac Surg
.
2009
;
38
:
201
209
.
22
Sándor
GK,
Numminen
J,
Wolff
J,
et al.
Adipose stem cells used to reconstruct 13 cases with cranio-maxillofacial hard-tissue defects
.
Stem Cells Transl Med
.
2014
;
3
:
530
540
.
23
Lendeckel
S,
Jödicke
A,
Christophis
P,
et al.
Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report
.
J Craniomaxillofac Surg
.
2004
;
32
:
370
373
.
24
Barba
M,
Cicione
C,
Bernardini
C,
Michetti
F,
Lattanzi
W.
Adipose-derived mesenchymal cells for bone regereneration: state of the art
.
Biomed Res Int
.
2013
;
2013
:
416391
.
25
Sierra-Johnson
J,
Johnson
BD.
Facial fat and its relationship to abdominal fat: a marker for insulin resistance?
Med Hypotheses
.
2004
;
63
:
783
786
.
26
Abuabara
A,
Cortez
A,
Passeri
L,
De Moraes
M,
Moreira
R.
Evaluation of different treatments for oroantral/oronasal communications: experience of 112 cases
.
Int J Oral Maxillofac Surg
.
2006
;
35
:
155
158
.
27
Alkan
A,
Dolanmaz
D,
Uzun
E,
Erdem
E.
The reconstruction of oral defects with buccal fat pad
.
Swiss Med Wkly
.
2003
;
133
:
465
470
.
28
Martín-Granizo
R,
Naval
L,
Costas
A,
et al.
Use of buccal fat pad to repair intraoral defects: review of 30 cases
.
Br J Oral Maxillofac Surg
,
1997
;
35
:
81
84
.
29
El Haddad
SA,
Abd El Razzak MY, El Shall M. Use of pedicled buccal fat pad in root coverage of severe gingival recession defect
.
J Periodontol
.
2008
;
79
:
1271
1279
.
30
Farré-Guasch
E,
Martí-Pagès
C,
Hernández-Alfaro
F,
Klein-Nulend
J,
Casals
N.
Buccal fat pad, an oral access source of human adipose stem cells with potential for osteochondral tissue engineering: an in vitro study
.
Tissue Eng Part C Methods
.
2010
;
16
:
1083
1094
.
31
Szpalski
C,
Barr
J,
Wetterau
M,
Saadeh
PB,
Warren
SM.
Cranial bone defects: current and future strategies
.
Neurosurg Focus
.
2010
;
29
:
E8
.
32
Clarke
A,
Flowers
MJ,
Davies
AG,
Fernandes
J,
Jones
S.
Morbidity associated with anterior iliac crest bone graft harvesting in children undergoing orthopaedic surgery: a prospective review
.
J Child Orthop
.
2015
;
9
:
411
416
.
33
Bednar
DA,
Al-Tunaib
W.
Failure of reconstitution of open-section, posterior iliac-wing bone graft donor sites after lumbar spinal fusion. Observations with implications for the etiology of donor site pain
.
Eur Spine J
.
2005
;
14
:
95
98
.
34
Kurz
LT,
Garfin
SR,
Booth
RE
Jr.
Harvesting autogenous iliac bone grafts: a review of complications and techniques
.
Spine
.
1989
;
14
:
1324
1331
.
35
Ahlmann
E,
Patzakis
M,
Roidis
N,
Shepherd
L,
Holtom
P.
Comparison of anterior and posterior iliac crest bone grafts in terms of harvest-site morbidity and functional outcomes
.
J Bone Joint Surg Am
.
2002
;
84
:
716
720
.
36
Khojasteh
A,
Sadeghi
N.
Application of buccal fat pad-derived stem cells in combination with autogenous iliac bone graft in the treatment of maxillomandibular atrophy: a preliminary human study
.
Int J Oral Maxillofac Surg
.
2016
;
45
:
864
871
.
37
Matarasso
A.
Buccal fat pad excision: aesthetic improvement of the midface
.
Ann Plast Surg
.
1991
;
26
:
413
418
.
38
Niada
S,
Ferreira
LM,
Arrigoni
E,
et al.
Porcine adipose-derived stem cells from buccal fat pad and subcutaneous adipose tissue for future preclinical studies in oral surgery
.
Stem Cell Res Ther
.
2013
;
4
:
1
.
39
Riachi
F,
Naaman
N,
Tabarani
C,
et al.
Influence of material properties on rate of resorption of two bone graft materials after sinus lift using radiographic assessment
.
Int J Dent
.
2012
;
2012
:
737262
.
40
Robinson
BT,
Metcalfe
D,
Cuff
AV,
et al.
Surgical techniques for autologous bone harvesting from the iliac crest in adults
.
Cochrane Database Syst Rev
.
2015
;
7
:
1
12
.
41
Sen
M,
Miclau
T.
Autologous iliac crest bone graft: should it still be the gold standard for treating nonunions?
Injury
.
2007
;
38
:
S75
S80
.
42
Goulet
JA,
Senunas
LE,
DeSilva
GL,
Greenfield
MLV.
Autogenous iliac crest bone graft: complications and functional assessment
.
Clin Orthop Relat Res
.
1997
;
339
:
76
81
.
43
Younger
EM,
Chapman
MW.
Morbidity at bone graft donor sites
.
J Orthop Trauma
.
1989
;
3
:
192
195
.
44
Smith
JD,
Abramson
M.
Membranous vs endochondral bone autografts
.
Arch Otolaryngol
.
1974
;
99
:
203
205
.
45
Akintoye
SO,
Lam
T,
Shi
S,
Brahim
J,
Collins
MT,
Robey
PG.
Skeletal site-specific characterization of orofacial and iliac crest human bone marrow stromal cells in same individuals
.
Bone
.
2006
;
38
:
758
768
.
46
Fujii
T,
Ueno
T,
Kagawa
T,
Sakata
Y,
Sugahara
T.
Comparison of bone formation ingrafted periosteum harvested from tibia and calvaria
.
Microsc Res Tech
.
2006
;
69
:
580
584
.
47
Zins
JE,
Whitaker
LA.
Membranous versus endochondral bone: implications for craniofacial reconstruction
.
Plast Reconstr Surg
.
1983
;
72
:
778
784
.
48
England
MA.
The developing human: clinically oriented embryology
.
J Anat
.
1989
;
166
:
270
.
49
Amini
AR,
Laurencin
CT,
Nukavarapu
SP.
Bone tissue engineering: recent advances and challenges
.
Crit Rev Biomed Eng
.
2012
;
40
:
363
408
.
50
Al-Salleeh
F,
Beatty
MW,
Reinhardt
RA,
Petro
TM,
Crouch
L.
Human osteogenic protein-1 induces osteogenic differentiation of adipose-derived stem cells harvested from mice
.
Arch Oral Biol
.
2008
;
53
:
928
936
.
51
Ahn
HH,
Kim
KS,
Lee
JH,
et al.
In vivo osteogenic differentiation of human adipose-derived stem cells in an injectable in situ-forming gel scaffold
.
Tissue Eng Part A
.
2009
;
15
:
1821
1832
.
52
Jurgens
WJ,
Oedayrajsingh-Varma
MJ,
Helder
MN,
et al.
Effect of tissue-harvesting site on yield of stem cells derived from adipose tissue: implications for cell-based therapies
.
Cell Tissue Res
.
2008
;
332
:
415
426
.
53
Amin
M,
Bailey
B,
Swinson
B,
Witherow
H.
Use of the buccal fat pad in the reconstruction and prosthetic rehabilitation of oncological maxillary defects
.
Br J Oral Maxillofac Surg
.
2005
;
43
:
148
154
.
54
Baumann
A,
Ewers
R.
Application of the buccal fat pad in oral reconstruction
.
J Oral Maxillofac Surg
.
2000
;
58
:
389
392
.
55
Stuzin
JM,
Wagstrom
L,
Kawamoto
HK,
Baker
TJ,
Wolfe
SA.
The anatomy and clinical applications of the buccal fat pad
.
Plast Reconstr Surg
.
1990
;
85
:
29
37
.
56
Sándor
GK,
Tuovinen
VJ,
Wolff
J,
et al.
Adipose stem cell tissue–engineered construct used to treat large anterior mandibular defect: a case report and review of the clinical application of good manufacturing practice–level adipose stem cells for bone regeneration
.
J Oral Maxillofac Surg
.
2013
;
71
:
938
950
.
57
Sleff
T,
Lehtimäki
K,
Niskakangas
T,
et al.
Cranioplasty with adipose-derived stem cells and biomaterial: a novel method for cranial reconstruction
.
Neurosurgery
.
2011
;
68
:
1535
1540
.
58
Mesimäki
K,
Lindroos
B,
Törnwall
J,
et al.
Novel maxillary reconstruction with ectopic bone formation by GMP adipose stem cells
.
Int J Oral Maxillofac Surg
.
2009
;
38
:
201
209
.