SURGICAL ONCOLOGY AND RECONSTRUCTION

Immediate Transoral Allogeneic Bone

Grafting for Large Mandibular Defects.
Less Morbidity, More Bone. A Paradigm
in Benign Tumor Mandibular
Reconstruction?
James C. Melville, DDS,* Nader N. Nassari, DDS,y Issa A. Hanna, DDS,z
Jonathan W. Shum, DDS, MD,k Mark E. Wong, DDS,{ and
Simon Young, DDS, MD, PhD#
Purpose: Reconstruction of hard tissue continuity defects caused by ablative tumor surgery has been
traditionally reconstructed with autogenous bone grafts or microvascular free flaps. Although results
have been predictable from these 2 methods of reconstruction, the morbidity associated with bone harvest
is quite serious for the patient. Predictable results have been obtained with using a combination of 100%
cadaver bone, bone marrow aspirate concentrate (BMAC), and recombinant human bone morphogenic
protein in immediate reconstruction for benign tumor extirpations through the extraoral approach. In
light of these successful outcomes, the same combination was evaluated with an intraoral approach.
This study evaluated the success of immediate mandibular reconstruction through the intraoral approach
without any autogenous bone harvesting.
Patients and Methods: The aim of this retrospective study was to share the authors’ experience with
the use of 100% allogeneic bone in combination with bone morphogenic protein and BMAC through the
transoral approach for immediate reconstruction of continuity defects that resulted from benign tumor
surgery. A retrospective chart review was performed of all patients undergoing bone graft reconstruction
at the University of Texas Health Sciences Center at Houston (UTHealth) Department of Oral and Maxillo-
facial Surgery from December 2014 through January 2016. Inclusion criteria were biopsy-proven benign
tumors, American Society of Anesthesiologists I or II health status, and adequate intraoral soft tissue for
primary closure determined during initial consultation.
Results: Five patients who underwent this procedure at the UTHealth Department of Oral and Maxillo-
facial Surgery from December 2014 through January 2016 are presented. The success rate was 100%. All
patients showed excellent bone quality clinically and radiographically for endosseous dental implant

Received from the University of Texas Health Sciences Center at
Houston, School of Dentistry, Houston, TX.
*Assistant Professor, Departments of Oral and Maxillofacial
Surgery and Oral, Head, and Neck Oncology, and Microvascular
Surgery.
yChief Resident, Department of Oral and Maxillofacial Surgery.
zAssistant Professor, Department of Oral and Maxillofacial
Surgery.
kAssistant Professor, Department of Oral and Maxillofacial
Surgery.
{Professor, Chair, and Program Director, Department of Oral and
Maxillofacial Surgery.
#Assistant Professor, Department of Oral and Maxillofacial
Surgery.
Conflict of Interest Disclosures: None of the authors have any
relevant financial relationship(s) with a commercial interest.
This work was presented as a Scientific Oral Abstract at the annual
meeting of the American Academy of Craniomaxillofacial Surgeons;
Ann Arbor, MI; May 20 to 21, 2016; and as a Scientific Poster at the
98th Annual Meeting of the American Association of Oral and Maxil-
lofacial Surgeons; Las Vegas, NV; September 22, 2016.
Address correspondence and reprint requests to Dr Melville: Uni-
versity of Texas Health Sciences Center at Houston, School of
Dentistry, 7500 Cambridge Street, Suite 6510, Houston, TX 77054;
e-mail: James.C.Melville@uth.tmc.edu
Received July 19 2016
Accepted September 29 2016
Ó 2016 American Association of Oral and Maxillofacial Surgeons
0278-2391/16/30911-9
http://dx.doi.org/10.1016/j.joms.2016.09.049

828
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MELVILLE ET AL 829

placement. With the transoral approach and no autogenous bone harvesting, the average operating time
was 3.4 hours and the hospital stay was 2.4 days.
Conclusions: Composite allogeneic tissue engineering is an effective and predictable technique for im-
mediate reconstruction of continuity defects from ablative benign tumor surgery. Overall, there was no
donor site morbidity, the intraoperative time was shorter, there were fewer admission days, and total costs
overall were lower compared with traditional methods.
Ó 2016 American Association of Oral and Maxillofacial Surgeons
J Oral Maxillofac Surg 75:828-838, 2017

Adequate reconstruction of continuity defects in the
mandible with good esthetic and functional results re-
mains one of the challenges in oral and maxillofacial
surgery. Over the years, several methods, such as
autogenous bone grafting, free fibula flap grafting,
and use of bone marrow aspirate concentrate
(BMAC) through extraoral approaches, have been
tried, with good outcomes. However, most of these
methods have their disadvantages, such as donor site
morbidity, multiple surgeries, and compromised
esthetics.1
Use of BMAC for bone regeneration in the mandible
has become an accepted and reliable method of
mandibular reconstruction.2 However, this technique
has been performed using an extraoral approach and
as a separate secondary reconstructive surgery. Most
reconstructive surgeons recommend waiting for com-
plete healing of intraoral surgical sites before defect
reconstruction using traditional nonvascularized
bone grafts in an extraoral approach.1,3-5 The
common belief is that exposure of the grafting site to
intraoral fluids and flora could compromise
grafting results.6
The authors attempted simultaneous grafting of
mandibular defects through intraoral incisions with
the use of BMAC, bone morphogenic protein (BMP),
and particulate bone allograft.
Patients and Methods
In accordance with the policy of the institutional
review board of the University of Texas Health Sci-
ences Center at Houston (UTHealth), the institutional
review board reviewed and approved this study. A
retrospective chart review was performed of all
patients undergoing bone graft reconstruction at
the UTHealth Department of Oral and Maxillofacial
Surgery from December 2014 through January
2016. Appropriate consent forms were obtained
from the patients described in this report. All these
patients were diagnosed with benign mandibular
tumors with no history of chemotherapy or radiation
to the mandible. Different treatment modalities,
including use of a vascularized free fibula flap, use
of an avascular autogenous bone graft, and composite
allogeneic tissue engineering, were discussed with
patients in detail. The risks and benefits of each treat-
ment option, such as donor site morbidity, length of
hospital stay, and length of surgery, were discussed
with patients. All patients elected to undergo recon-
struction with composite allogeneic tissue engineer-
ing (Table 1).
Patients’ inclusion criteria for implant treatment
were 1) biopsy-proven benign tumor, 2) American
Society of Anesthesiologists I or II physical status,
3) clinically determined adequate soft tissue for
primary closure, 4) no history of chemotherapy or
radiation to the mandible, and 5) patients who
elected the tissue-engineered graft vs the free
vascular flap vs the autogenous bone graft with or
without BMP.
Patients’ exclusion criteria were 1) patients with
poor prognosis or systemically compromised health,
2) patients with extensive soft tissue involvement of
tumor, 3) patients with malignant disease, and 4) non-
compliant patients or patients who preferred autoge-
nous or free flap reconstruction.
Results
This retrospective study describes 5 patients who
were treated at the UTHealth Department of Oral
and Maxillofacial Surgery from December 2014
through January 2016. The length of defects in these
patients ranged from 3.5 to 8.0 cm. All patients were
diagnosed with benign lesions of the mandible.
BMAC was harvested from the bilateral anterior iliac
crest or the unilateral posterior iliac crest. The oper-
ating time was 3.4 hours on average and the length
of hospital stay was 1 to 5 days (average, 2.5 days).
Of the 5 patients, 4 were left in intermaxillary fixation
(IMF) for 3 weeks and 1 patient was not placed in IMF
because of a history of obstructive sleep apnea. All pa-
tients developed moderate postoperative swelling
associated with the use of BMP, with no airway
compromise, which markedly improved after the first
2 weeks postoperatively. All patients could return to
work at 3 weeks after their surgery. The freeze-dried
cortical and cancellous bone in combination with
large recombinant human BMP-2 (rhBMP-2; 12 mg)
with an absorbable collagen sponge and BMAC
120 mL obtained from the anterior or posterior hip

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830 BONE GRAFTING FOR LARGE MANDIBULAR DEFECTS

Table 1. PATIENTS WHO UNDERWENT RECONSTRUCTION OF THEIR MANDIBLE WITH COMPOSITE GRAFTING

Patient ASA
Number Gender Age (yr) MH Medications Smoking Habit Classification

1 Male 18 Childhood petite mal seizures None Nonsmoker II

2 Male 66 HTN, GERD, melanoma, Doxazosin, finasteride, Zantac Nonsmoker II
BPH, OSA
3 Female 58 HTN HCTZ, metoprolol, amlodipine Nonsmoker II
4 Female 36 None None Smoker I
5 Male 34 None None Nonsmoker I

Note: Patients’ ages ranged from 18 to 66 years. There were 3 men and 2 women and none of them had a severe systemic in-
capacitating medical problem. Only 1 patient was a current smoker who continued to smoke during her recovery period.
Abbreviations: ASA, American Society of Anesthesiologists; BPH, benign prostatic hyperplasia; GERD, gastroesophageal reflux
disease; HCTZ, hydrochlorothiazide; HTN, hypertension; MH, medical history; OSA, obstructive sleep apnea.
Melville et al. Bone Grafting for Large Mandibular Defects. J Oral Maxillofac Surg 2017.

were mixed homogeneously and used as the grafting
composite. The traditional formula of crushed cortical
and cancellous bone 10 mL was used for each 1-cm
length of defect (Table 2).
After resection of the lesion and then grafting, soft tis-
sue closure should not be under tension. Glycopyrro-
late 0.2 mg was given 15 minutes before placement of
the bone graft to minimize saliva pooling. Peridex
0.12% was poured into the defect site for a minute
and then irrigated with saline thoroughly to decrease
bacterial load in the graft site. A crib for the bone
mixture was composed of a titanium mesh or a poly(L-
lactide) or poly(D,L-lactide) reabsorbable mesh (the
latter has the advantage of being biodegradable).
A small strip of BMP and a gel-like mixture composed
of platelet-poor plasma, calcium chloride, and thrombin
is placed underneath the mucosa before closure to pro-
mote faster soft tissue healing.7 Suturing technique and
suture material used for closure play a major part in
achieving a water-tight seal in the soft tissue. The au-
thors’ preferred technique for closure is a running verti-
cal mattress suture with 3-0 Prolene suture oversewn
with 3-0 chromic gut suture in an interrupted or contin-
uous fashion. A thin layer of Dermabond was placed to
act as a temporary sealant around questionable margins
such as around teeth (Fig 1A, B).
The authors looked at several criteria from a func-
tional and esthetic standpoint to evaluate the success

Table 2. INFORMATION ABOUT LESIONS AND SURGERIES

Length of
Patient Length of Pathologic Hospital BMAC Harvest Site/
Number Location of Defect Defect (cm) Diagnosis IMF (wk) Stay (days) Amount (mL)

1 Left body of mandible to 8.0 Ossifying fibroma 3 5* Bilateral anterior iliac

condyle* crest/120
2 Anterior mandible and 3.5 Desmoplastic 0 (from OSA) 1 Right posterior iliac
left body of mandible ameloblastoma crest/120
3 Right posterior body of 6.2 Ameloblastomay 5 2 Right posterior iliac
mandible crest/120
4 Anterior mandible and 5.4 Juvenile ossifying 3 2 Bilateral anterior iliac
right body of mandible fibroma crest/120
5 Anterior mandible and 10.1 Ameloblastoma 3 2 Bilateral anterior iliac
left body of mandible crest/120
extending past the left
mandibular third molar

Abbreviations: BMAC, bone marrow aspirate concentrate; IMF, intermaxillary fixation; OSA, obstructive sleep apnea.
* The lesion in this patient extended to the left ramus of the mandible and condylar head and required disarticulation of the left
condyle and costochondral graft to reconstruct the left condyle.
y Patient underwent marginal resection of the mandible and the inferior border was left intact.
Melville et al. Bone Grafting for Large Mandibular Defects. J Oral Maxillofac Surg 2017.

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MELVILLE ET AL 831

FIGURE 1. A, Schematic of surgical placement of tissue-engineered components immediately after resection. Diagram courtesy of Dr Daniel J.
Stackowicz. B, Surgical image of intraoral graft placement. BMAC, bone marrow aspirate concentrate; BMP, bone morphogenic protein.
Melville et al. Bone Grafting for Large Mandibular Defects. J Oral Maxillofac Surg 2017.

rate in this group of patients. Complete bony union at

the site of the defect was the main goal in all cases.
Bony union was determined by radiographic examina-
tion to evaluate the margin between the bone graft and
the remaining mandible. A minimum height of 2 cm
and a minimum width of 1 cm at the grafted site
were the success criteria for bone regeneration at
the defect. The authors evaluated the quality of newly
formed bone for placing an endosteal dental implant in
the site with good initial stability to meet the patients’
desire of having teeth for function and esthetics. The
authors believe that the reconstructed bone should
be implantable to achieve this goal for a fixed or
removal prosthesis. Maintenance of the bony contour FIGURE 2. Histology of bone taken from patient 2 during implant
placement shows normal reactive bone with a regular trabecular
and adequate volume for 12 months postoperatively pattern with fibrosis and no remnants of cadaver bone after 8 months
was another aspect monitored by radiographic and (hematoxylin and eosin stain; magnification, 10).
clinical examination every 4 months to check for reab- Melville et al. Bone Grafting for Large Mandibular Defects. J Oral
sorption or infection of the reconstructed mandible. Maxillofac Surg 2017.

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832 BONE GRAFTING FOR LARGE MANDIBULAR DEFECTS

FIGURE 3. Patient 1. A, Preoperative cone-beam computed tomogram. B, Postoperative cone-beam computed tomogram.
Melville et al. Bone Grafting for Large Mandibular Defects. J Oral Maxillofac Surg 2017.

Acceptable restoration of facial form with a good
esthetic result was another factor included in the suc-
cessful mandibular reconstruction criteria for this
method. This criterion was defined by evaluating the
facial symmetry of the patient and the subjective
opinion of the patient.
The authors achieved 100% success after finding the
formation of complete bony union at the defect site.
Four patients had en bloc resection of the mandible,
1 of whom underwent disarticulation of the condyle
and reconstruction with a costochondral graft in
addition to the composite allogeneic tissue engineer-
ing. The other patient had marginal resection of his
mandible. All these patients showed adequate
bone formation in the defect site, which restored
mandibular continuity. As of July 2016, 2 of the 5 pa-
tients received dental implants. The other 3 patients,
because of financial restrictions, chose to have a
removable partial denture and decide in the future
whether they might want dental implants.
Patients underwent cone-beam computed tomo-
graphic (CBCT) scanning at their 8- to 12-month
follow-up appointments. Based on measurements
from the CBCT scan, regenerated bone width was 10
to 14.5 mm and regenerated bone height was 22 to
26 mm in patients with en bloc resection. The single
patient with a marginal resection had an additional
15-mm height of bone regenerated in addition to the
remaining 10 mm of native bone. Good bone density
was visualized on CBCT scans in all cases. All patients

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MELVILLE ET AL 833

FIGURE 4. Patient 2. A, Preoperative cone-beam computed tomogram. B, Postoperative cone-beam computed tomogram.
Melville et al. Bone Grafting for Large Mandibular Defects. J Oral Maxillofac Surg 2017.

were happy with the esthetic result of their operation
and were looking forward to their dental rehabilita-
tion. None of the patients had an extraoral scar, which
is one of the advantages of this technique compared
with previous methods (Figs 2-8, Table 3).
Discussion
It has been more than 50 years since Urist8 first
described BMP and a decade and a half since Mogha-
dam et al3 first described the use of BMP for mandib-
ular reconstruction in a human model in 2001.
Through multiple studies, BMP has shown its efficacy,
safety, and predictability when combined with osteo-
conductive and osteogenic components in mandibular
reconstruction.9,10 The traditional method of
mandibular reconstruction, which uses the
allogeneic tissue-engineering protocol, has been per-
formed as a staged secondary procedure.9 The reason
for the secondary grafting is to achieve complete oral
healing and perform grafting through an extraoral
approach to eliminate graft site contamination. Some
benign tumors can be removed entirely through the in-
traoral approach without a transcervical incision. The
question then becomes, how can one treat patients
with 1 surgery only, avoid an extraoral incision, elimi-
nate donor site morbidity, and obtain predictable
results? Pogrel et al10 compared the vascularized free
flap with autogenous bone grafting for large defects
and found that although the microvascular free flaps
were more successful (95 vs 76%), these patients
stayed an average of 14 additional days in the hospital.

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834 BONE GRAFTING FOR LARGE MANDIBULAR DEFECTS

FIGURE 5. Patient 3. A, Preoperative cone-beam computed tomogram. B, Postoperative cone-beam computed tomogram.
Melville et al. Bone Grafting for Large Mandibular Defects. J Oral Maxillofac Surg 2017.

Schlieve et al11 reported 18 of 20 patients had success-
ful reconstruction using an intraoral technique with
autogenous anterior iliac crest bone grafting.12 One
also must take into account the donor site morbidity
with free composite flaps13,14 and avascular bone
harvesting. The question at this point is, can
immediate reconstruction of mandibular continuity
defects be performed reliably and predictably after
benign tumor extirpation with composite allogeneic
tissue engineering?
Before delving in this further, the fundamental prin-
ciples of tissue engineering should be discussed.
There are 3 essential factors that need to be
considered in a tissue-engineering approach. First,
scaffolding is provided by the allogeneic bone, which
acts as a framework for bone regeneration. Second,
signaling for regeneration is provided by rhBMP-2,
which promotes differentiation of the stem cells and
migrating osteogenic cells.15 Third, regenerative cells
are provided by BMAC and migrating osteogenic cells.
The combination of all these factors leads to bone
regeneration. The use of BMP for mandibular recon-
struction is strictly off-label, and the patient must be
informed and consent to off-label use. The Food and
Drug Administration has approved only maxillary si-
nus augmentation and augmentations for defects asso-
ciated with extraction sockets.
Bone marrow aspirate serves as the richest and most
readily available source of these bone-forming cells,16
which otherwise would not be present in sufficient
quantities, and is easily harvested and concentrated
without serious donor site morbidity.17 Multiple
studies have shown that bone marrow–derived stem
and progenitor cells regenerate bone in animal18 and

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MELVILLE ET AL 835

FIGURE 6. Patient 4. A, Preoperative cone-beam computed tomogram. B, Postoperative cone-beam computed tomogram.
Melville et al. Bone Grafting for Large Mandibular Defects. J Oral Maxillofac Surg 2017.

human18,19 models. BMAC has been used frequently
and regularly with spine surgery,20 orthopedic sur-
gery,21,22 and myocardial regeneration.23 Marx and
Harrell2 found that CD34+CD44+CD90+CD105+ cells
constitute the main osteoprogenitor population
collected in the BMAC.
The 5 patients included in this report had different
age ranges with various benign pathologic diagnoses.
All patients had a successful outcome according to
the noted criteria. Patients involved in this study
were diagnosed with relatively large benign lesions
of the mandible. In the past, similar defects have
been treated with more invasive methods of recon-
struction after resection of lesions. These more inva-
sive methods resulted in less esthetic outcomes
because of the presence of extraoral incisions and

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836 BONE GRAFTING FOR LARGE MANDIBULAR DEFECTS

FIGURE 7. Patient 5. A, Preoperative cone-beam computed tomogram. B, Postoperative cone-beam computed tomogram.
Melville et al. Bone Grafting for Large Mandibular Defects. J Oral Maxillofac Surg 2017.

scarring, longer hospital stays because of potential

donor site morbidity, and more complex immediate
postoperative care. With the method of immediate in-
traoral reconstruction of these defects, none of these
patients’ surgeries required an extraoral incision.
This eliminated unesthetic neck scars. All patients
had proper facial contour restored after
reconstruction.
After intraoral reconstruction of the mandibular de-
fects, 4 patients had a hospital stay shorter than
48 hours postoperatively. In contrast, 1 patient had
an extended hospital stay of 5 days, because of postop-
erative anxiety and inadequate oral intake. The
FIGURE 8. Placement of dental implants in patient 5. Alveolar
average postoperative hospital stay for the 4 patients ridge exhibits excellent height and width for placement of 4-  5-
was 2 days 12 hours, which is still an improvement  13-mm implants.
compared with the average postoperative hospital Melville et al. Bone Grafting for Large Mandibular Defects. J Oral
stay for more invasive reconstructive options. Maxillofac Surg 2017.

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MELVILLE ET AL
Table 3. POSTOPERATIVE RESULTS
Patient 1
Bone width (mm) 11
Bone height (mm) 23
Months postoperatively 12
Implant placed Noy
* This is in addition to the remaining bone in the inferior border of the mandible, which was 1 cm.
y All patients were given the option of implants after 6 months, but 3 of 5 declined because of financial restrictions.
Melville et al. Bone Grafting for Large Mandibular Defects. J Oral Maxillofac Surg 2017.
To use the intraoral composite allogeneic tissue-
engineering technique, certain criteria have to be
considered. Lesions have to be resectable through
an intraoral approach with minimum to no soft tis-
sue involvement. Other questions to be investigated
further are the role of IMF in bone regeneration and
the effect of various postoperative diets. Postopera-
tive fixation and immobilization of the grafted site
has been recommended when extraoral approaches
are used for reconstruction.24 However, the abso-
lute need for such measures needs to be investi-
gated further. In addition, a consideration of
limiting patients’ diet to clear liquid for the first 2
to 3 postoperative days and slowly advancing to a
full liquid diet in a course of a week versus use of
the Dobhoff tube as a feeding access for nutrition
during the first immediate postoperative week are
potential solutions to minimizing possible graft
site contamination.
Considering the results from this case series, intrao-
ral reconstruction of large mandibular defects after
resection of benign lesions, with the use of BMAC,
rhBMP-2, and allogeneic bone, is an alternative to
more invasive methods of reconstruction and all but
obviates autogenous bone in these scenarios. It can
result in an improved esthetic outcome with less co-
morbidity and greater patient satisfaction. This tech-
nique is an evolving treatment modality and
additional data with larger patient populations are
needed. It is the intent of the authors to stimulate sur-
gical interest in this treatment modality and outcome-
based success might add an option in the treatment of
similar lesions.
Acknowledgment
The authors thank the various oral and maxillofacial surgical res-
idents and dental students at the UTHealth School of Dentistry for
their contributions to this article: Dr Jeanette Johnson (third-year
resident), Dr Daniel J. Stackowicz (second-year resident, Kim
Nguyen (first-year dental student), Dr Matthew Breit (second-year
resident), Dr Rodolfo ‘ Rudy’’ Garza (chief resident), and Dr Steven
Shen, MD, PhD (Houston Methodist Hospital Department of Pathol-
ogy). They also personally thank Dr Robert E. Marx for stimulating
interest in tissue engineering for maxillofacial reconstruction.
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837
Patient 2 Patient 3 Patient 4 Patient 5
10 10 14.5 15
23* 26* 21.9 29
13 12 12 14
Yes Noy Noy Yes
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