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21 Bone andCartilage Tissue Engineering andRegenerative Medicine inCraniofacial Surgery
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Oral Mucosa Tissue Engineering
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inCraniofacial Surgery
GünterLauer
22
Introduction
In the craniofacial region, tissue decits or
defects can result from facial deformities, trauma,
chronical infections (e.g., loss of teeth and alveolar bone due to periodontitis), or ablative tumor
surgery. Depending on the size and the type of
tissue lacking, different strategies are pursued, in
order to replace the structures adequately. Bony
structures may be replaced suitably by different
types of bone grafts, e.g., local grafts from the
mandible or maxilla, free grafts from the hip, or
even microvascular free aps from the bula or
the lower forearm, but also by bone replacement
materials or even tissue-engineered bone [1–5].
However, if soft tissue is missing particularly
in the oral cavity, there is always the need to have
an adequate oral mucosa lining. Especially
around teeth or dental implants, the oral mucosa
coverage should be rmly attached to the bone
and ideally be keratinized. As the source for oral
mucosa is limited, free split skin transplants or, in
case of extended defects, microvascular free aps
like the radial forearm ap, the lateral upper arm
ap, the rectus abdominis ap, or the latissimus
dorsi ap may be used instead [6–8]. These
approaches take a certain mist as disadvantage
by replacing mucosa with skin, which may lead
G. Lauer (*)
Department for Oral and Maxillofacial Surgery,
University Hospital Dresden, Dresden, Germany
e-mail: Guenter.Lauer@uniklinikum-dresden.de
to hyperkeratosis and/or hyperproliferations.
Only if split skin grafts are harvested very thinly
may the results be as good as when transplanting
split mucosa grafts [9]. Thus, in oral and craniofacial reconstruction, there is a denite need for
mucosa grafts.
Since the advent of cell culture and tissue
engineering, there has been efforts to create
mucosa grafts and to apply them in the clinical
setting. In the following, the way from cell culture to tissue engineering of oral mucosa is
described and examples for the clinical application of this oral epithelial tissue are given.
Moving fromCulturing Oral
Keratinocytes toTissue Engineering
ofOral Mucosa
Culture ofEpithelial Cells, 3T3
Fibroblasts
The cultivation of adult mammalian skin cells
had been described more than 70years ago [10].
The co-culture with mouse broblasts and the
use of epidermal growth factor allowed for sufcient keratinocyte proliferation [11, 12] and the
culturing of epithelial sheets in bulk enabling
their clinical application. In the early 1980s, the
rst reports using keratinocyte sheets as transplant in the treatment of large burns were published [13, 14]. Ten years later, the rst clinical
© Springer Nature Switzerland AG 2023
U. Meyer (ed.), Fundamentals of Craniofacial Malformations,
https://doi.org/10.1007/978-3-031-28069-6_22
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application of cultured oral mucosa cells—still
cultured with 3T3 mouse feeder cells and fetal
calf serum—was pioneered in tumor-related surgery and periodontal surgery [15–17]. However,
these conditions for culturing primary epithelial
cell grafts were not suitable to grow transplants
for use in elective surgery. To adapt the culture
conditions for grafts used in elective surgery, the
explant culture technique and the use of
autogenous serum instead of fetal calf serum
were introduced.
Explant Culture ofGingival
Keratinocytes
To omit transfection of the human cells by murine
DNA components from the 3T3 mouse feeder
cells, primary gingiva epithelial cultures can be
established using the explant culture technique
[18–20]. Therefore, after removing the connective tissue from the biopsies, the remaining epithelial tissue was divided in 1 mm explants,
seeded on plastic petri dishes, and covered with
little culture medium. From these explants, the
keratinocytes migrate onto the culture dish and
proliferate further (Fig.22.1a–c). The efcacy of
this explant technique for establishing cultures
has been conrmed in several studies comparing
it to establishing cultures from single-cell suspensions [19, 21, 22].
Autogenous Serum
Serological investigations on patients with burns
and after transplantation of cultured skin keratinocytes revealed that they developed antibodies
against bovine serum proteins [23]. This is a further imponderability, which patients undergoing
elective surgery, e.g., pre-prosthetic, periimplant, and periodontal surgery, should not be
exposed to. Therefore, in an intraindividual comparison, autogenous and fetal calf serum as
growth supplements was tested on gingival keratinocyte cultures. Within gingival keratinocyte
cultures of each patient, autogenous and fetal calf
serum had the same efcacy to promote cell
growth as assessed planimetrically by cellcovered surfaces after 24days [24].
Patient Age, Senescence ofCultured
Cells
Reconstructive procedures requiring mucosa
grafts, e.g., pre-prosthetic and peri-implant surgery, are performed usually in older patients. In
this respect, it is interesting to compare the
growth and proliferation potential in gingival
keratinocyte explant cultures from patients
younger and older than 40 years of age. DNA
synthesis rate and DNA content, as parameters
for epithelial growth, were determined. The DNA
a b c
Fig. 22.1 (a) Explant on the oor of the culture dish with
outgrowth of epithelial cells. On the layer of adherent
keratinocytes, there are epithelial cells migrating. Light
microscopic picture, magnication ×400. (b) Culture
ask covered with a dense layer of oral keratinocytes.
Epithelial cell growth has started from the small tissue
explants in the center of the ask. (c) Culture asks after
6, 9, 12, and 24 days of culture (left to right). There,
islands of oral keratinocytes which nally form a conuent dense layer
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synthesis rate (proliferation) in cultures of
younger patients is signicantly higher between
days 8 and 12, whereas in cultures of older
patients, the proliferation peaks between days 24
and 28. Total cell growth was also higher in cultures of younger patients as the DNA content
measured over the whole culture period was 2/3
higher. Although there is a clear age dependency,
it is possible to culture gingival keratinocytes
from old patients in sufcient amounts [22].
After a period of 40–60days, the primary epithelial cultures started to disintegrate.
Keratinocytes detached from the culture dish and
the remaining cells lost their cobblestone shape.
Oral keratinocytes could only be subcultured
once, ideally between days 14 and 21 of culture
when there was a high proliferation rate.
Tissue Engineering ofOral Mucosa
Grafts
To tissue engineer mucosa grafts, small gingival
biopsies (max. 6 mm diameter) were dissected
into the epithelial layer (keratinocytes) and connective tissue (broblasts). At the beginning,
only the epithelial layer was cultured and therefore cut into small explants. The connective tissue was discarded. Autogenous serum, which had
been extracted from venous blood by centrifugation, was added to the culture medium. After
3–5 days, the gingival keratinocytes migrated
from the explants onto the oor of culture dish
developing epithelial islets which expanded radially forming conuent gingival epithelial layers
(Fig. 22.1a, b). In the original approach, after
approx. 21 days, the epithelial cell layer of the
primary culture was detached by the enzyme dispase and then attached to Vaseline gauze as a carrier (Fig. 22.5a, b). Keratinocytes plus carrier
were transplanted onto the dissected wound site
of the patient as originally used for skin keratinocyte grafts [14].
To simplify the intraoperative handling of
these cultured gingival keratinocyte sheets, carrier materials like collagen membranes, polylactide foils (Fig. 22.2a, b), and Vicryl nets were
tested to act as a carrier material instead of the
Vaseline gauze. In these tests, primary gingival
keratinocyte cultures were dissolved into singlecell suspension after 14–21days, seeded onto the
carrier materials in a density of 20,000–
50,000 cells/cm2, and cultured in DMEM and
KCSFM 1:1 with the specic additives (Gibco
Inc., Eggenstein, Germany). This period of time
was considered as optimum to obtain a maximum
amount of epithelial cells in relation to their proliferation activity [22, 25]. The cells adhered well
to the different materials forming an epithelial
layer [26, 27]. After another 2–3days, and a total
culture time period of approx. 4weeks, epithelial
constructs, consisting of two to three cell layers
ab
Fig. 22.2 (a) Light microscopic picture of a sheet of cul-
tured oral keratinocytes detached from the culture with
the enzyme dispase in order to be used as an autogenous
graft (see also Fig. 22.5a, b). Richardson Blue staining,
magnication ×600. (b) Polylactide foil with a layer of
adherent oral keratinocytes. The cytoplasms of the keratinocytes have a at shape. Light microscopic picture, HE
staining, magnication ×400
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G. Lauer
on carrier materials (Fig.22.2a, b) and with a size
of up to 15cm2, were ready for transplantation.
For epithelial cells of other origin, similar results
on different biomaterials [28] could be observed.
The Tissue-Engineered Oral
Keratinocyte-Fibroblast Graft
Split mucosa grafts consist of a layer of epithelial cells on a brous connective tissue component containing broblasts. In order to imitate
this structural composition, there are reports to
add an acellular allogenic dermal matrix
(AlloDerm®) as the connective tissue part, thus
creating an exvivo-produced oral mucosa equivalent (EVPOME) [29, 30]. However, there are
in vivo in transplantation studies as well as
in vitro investigations that emphasize on the
importance of living broblasts within the submucosa connective tissue matrix [31–34].
Therefore, instead of discarding the connective
tissue, it was digested and broblasts were isolated and cultured in DMEM culture medium in
a concentration of 10,000 cells per ml. After
14–21days, the broblasts were trypsinized and
seeded as single-cell suspension into the collagen sponges. After incubating the collagen
sponges with broblasts overnight, they were
coated with a suspension of the oral keratinocytes. The schematic drawing gives a general
overview of this procedure to tissue engineer the
gingival keratinocyte graft (Fig. 22.3). After a
culture period of another 2 days, the tissueengineered oral keratinocyte-broblast graft was
ready for transplantation. The graft now consisted of layers of keratinocytes on a sponge
inhabited by broblasts (Fig.22.4).
Tissue Engineering Oral Mucosa
sy
Microdissecon
of biopsy
Fig. 22.3 Schematic drawing of the tissue engineering of
an oral keratinocyte-broblast graft. (a) The biopsy consists of epithelial tissue and broblast connective tissue.
(b) Microdissection of the biopsy into an epithelial part
and a connective tissue part. (c) The epithelial tissue is cut
into small explants and placed on the culture dish. The
keratinocytes start to migrate on the culture dish. In the
Oral Fibroblast Culture
B
io
Keranocyte Fibroblast Constructs
test tube, the broblasts are dissolved from the connective
tissue and afterwards seeded into the culture dish. (d)
After the broblasts and the keratinocytes have multiplied
in separate culture dishes, the broblasts are seeded into
the collagen sponge and the keratinocytes onto the collagen sponge to tissue engineer the oral keratinocytebroblast graft
22 Oral Mucosa Tissue Engineering inCraniofacial Surgery
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Fig. 22.4 Light microscopic picture of a tissueengineered oral keratinocyte-broblast graft. The collagen sponge is covered with a layer of oral keratinocytes.
The cytoplasms of the keratinocytes have a very at
shape. Within the pores of the sponge, there are broblasts. Light microscopic picture, Masson Goldner trichrome stain, magnication ×400
Surgical Applications ofTissueEngineered Oral Keratinocyte
Grafts
The clinical studies using the tissue-engineered
mucosa grafts were approved by the Ethic
Committees of Dresden University and Freiburg
University (15022002, 94/99). Since 1991, cultured autologous oral mucosa and tissueengineered oral mucosa were used primarily in
pre-prosthetic surgical procedures like vestibuloplasty and lowering the oor of the mouth,
freeing of the tongue, as well as periodontal surgery. Further, tissue-engineered mucosa grafts
were also used in oral and maxillofacial plastic
reconstructive procedures after tumor resection
in the head and neck region to prelaminate the
radial free forearm ap and also in urologic surgery [35, 36].
Vestibuloplasty andLowering
theFloor oftheMouth
Vestibuloplasty and lowering the oor of the
mouth are performed to create loco stabile, ideally keratinized mucosa around dental implants
and to extend the denture-bearing area. Hereby,
303
peri-implant soft tissue inammation with hyperproliferation, e.g., after grafting of skin [37],
should be avoided and the long-term survival of
implants improved [38]. The surgical approach
and technique used in these pre-prosthetic surgical procedures did not differ from that used in
conventional open vestibuloplasty or lowering
the oor of the mouth [39, 40]. However, after
dissection, the wound surface was covered by the
tissue-engineered transplant (Fig. 22.5a, b),
which was xed in place with a wound dressing
plate.
In a clinical follow-up study, the healing of
the tissue-engineered oral keratinocyte graft
was investigated on 42 patients with anterior
localized vestibuloplasty (Fig.22.5c, d) and on
25 patients with vestibuloplasty combined with
the lowering of the oor of the mouth. After
7days, when removing the protective plate, the
wound surface tended to bleed easily when
touched. Ten days after grafting, there was a
pale pink still vulnerable surface. The wound
generally stabilized within the next few days
and healed after 20 days. Up to 50 days after
grafting, the complete grafted surfaces were
stable, showing keratinization. After 6 months
to 1year, the texture of the grafted tissue area
had changed. There was a rim of keratinized tissue close to the alveolar crest, whereas there
was a non-keratinized mucosa towards the scar
line in the vestibule (Fig.22.5d). The scar line
determined the former caudal border of the tissue dissection.
The depth of the vestibule—the distance
between this white scar line and the alveolar
crest—was used as wound shrinkage parameter
of the grafted area in the long-term clinical follow- up [41]. It was monitored in the region of the
former teeth 45, 43, 41, 31, 33, and 35 after 1 and
4weeks, 6 and 12months, and after more than
60months for up to 10years. As the sign of the
initial wound shrinkage, the depth of the vestibule decreased considerably within the rst
6 months post-operation. Then the decrease
ceased at this level, and further reduction of the
vestibule depth was little as seen within the
observation period of up to 12years (Fig.22.6).
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a
c
Fig. 22.5 (a) Sheet of keratinocytes detached from the
culture dish and attached to a Vaseline gauze. (b) The
Vaseline gauze with keratinocytes attached is covering the
wound site after performing an anterior open vestibuloplasty. (c) Anterior vestibulum/mouth prior to vestibulo-
b
d
plasty. (d) Anterior lower jaw area 5 years after
vestibuloplasty and transplantation of tissue-engineered
oral mucosa. There is keratinized mucosa directly around
the implants but also an area of non-keratinized mucosa
between the scar line and the keratinization
Freeing oftheTongue
The freeing of the tongue operation with grafting
of tissue-engineered mucosa helps to improve
movement of the tongue and subsequently food
intake and swallowing in patients suffering from
the changed anatomy after ablative tumor surgery. After a disease-free interval of 6–12months,
freeing of the tongue was performed and the
wound healing and graft take as well as the functional improvement was assessed in ten patients.
In these cases, the grafts were secured by an
intraoral gauze dressing xed to the wound by
single-suture loops for 8–10days.
When removing the wound dressing, an epithelialized wound surface covered with some
brin was observed in all patients except for one.
In the other nine patients, a complete mucosal
layer had formed by 15–18days postoperatively,
and there was only some shrinkage of the wound
surface and attening of glossoalveolar sulcus
observed, but the primary improvement in tongue
mobility was maintained during the entire postoperative follow-up. There was a good improvement of speech in seven patients, and
prosthodontic restorations mainly implant borne
were possible in eight patients [42].
Prelaminating theRadial
ForearmFlap
The fascio-cutaneous radial forearm ap (RFF)
introduced by Yang etal. (1981) [43] has become
the packhorse in reconstructive oral and maxillofacial surgery using microvascular anastomosed
transplants [8]. Besides the donor-site morbidity, a
disadvantage in intraoral reconstruction is the transplantation of skin into the oral cavity. To overcome
this, the prelamination with mucosa has been suggested although the source of mucosa is very limited [36, 44]. To further improve this approach, in
ve patients, autogenous tissue- engineered mucosa
was used for the prelamination of the RFF. Oral
-12
-10
Vesbule depth in the different regions of the dental arch
1 week
4 weeks 6 months 1 year
> 5 years
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0
-2
-4
-6
-8
45 43 41 31 33 35
Fig. 22.6 Graph showing the decrease of depth of the vestibulum over years. The shrinkage was initially within the
rst months much stronger and ceased at a level that was stable over a period of up to 12years
a b
Fig. 22.7 (a) Intraoperative situs when harvesting the
radial forearm ap prelaminated with tissue-engineered
oral mucosa. (b) Defect at the inner cheek covered with a
mucosa cell transplants were cultured for 3weeks
as described above and implanted subcutaneously
at the lower forearm via a longitudinal incision,
where the RFF is going to be harvested. After
1 week, the RFF prelaminated with tissue-engineered mucosa was raised with the vascular pedicle and transplanted intraorally in the recipient
prelaminated radial forearm ap with tissue-engineered
oral mucosa
site followed by the microvascular anastomosis
(Fig.22.7a). The donor site was closed primarily
using the local skin. Intraorally, a maximum surface area of 6×8cm could be covered using the
prelaminated RFF [36]. During the further followup, a certain shrinkage of the prelaminated aps
was observed (Fig.22.7b).
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Surgical Applications ofTissueEngineered Oral KeratinocyteFibroblast Grafts
play an important role in the differentiation of
epithelial cells [32–34]. Therefore, the clinical
impact of the tissue-engineered oral keratinocytebroblast graft on the development of keratinized
The clinical follow-up using tissue-engineered
oral mucosa grafts in vestibuloplasties has shown
that there is wound shrinkage and loss of keratinization in the transplanted area over months and
years (Figs.22.5d and 22.6). It was demonstrated
that submucosal connective tissue and broblasts
mucosa was studied. In these patients, a vestibuloplasty was performed to condition the soft tissue on the alveolar ridge during implant insertion
or to extend the gingiva around teeth (Figs.22.8a
and 22.9a, c). The epiperiosteal wound surface
was covered with tissue-engineered oral
abc
Fig. 22.8 (a) Recession and lack of attached mucosa at
the lower front teeth. (b) Periodontal open vestibuloplasty
covered with tissue-engineered mucosa, which consists of
oral broblasts and oral keratinocytes in a collagen
sponge. (c) Clinical situation 1 year after grafting of
tissue- engineered oral mucosa (keratinocytes and broblasts). The rim of attached mucosa is increased
a
c
Fig. 22.9 (a) Clinical situation in the oral cavity after trau-
matic loss of the lower incisors; there is no attached mucosa
on the alveolar ridge. (b) Intraoperative situs: Vestibuloplasty
with an epiperiosteal dissection is performed. The tissueengineered oral keratinocyte- broblast grafts are placed on
the wound bed. (c) The lost teeth are replaced by dental
b
d
implants. (d) Clinical situation 4years after grafting of tissue-engineered oral keratinocyte- broblast graft consecutive placement of dental implant and prosthodontic
treatment with a xed bridge. There is stable keratinized
mucosa—gingival mucosa—around the dental implants
without any clinical signs of inammation
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mucosa. The clinical feature was conrmed in
biopsies. Histological controls showed a cornied epithelium with rete ridges (Fig. 22.10) as
well as the expression of cytokeratins 1, 2, 10,
and 11 immunohistologically.
Conclusion
Studies on tissue engineering of oral mucosa and
its application as graft in craniofacial surgery
have been shown to be a reliable technique to
replace conventional mucosa grafts in certain
types of surgery, particularly vestibuloplasty
around implants and periodontal surgery.
Advantage is that the limitation in the availability
of mucosa grafts may be overcome. However, an
issue that hinders the use of tissue-engineered
oral mucosa in a wider eld is the hurdles that
have been imposed by the legislation in 2007
making tissue engineering to a pharmaceutical
process.
Fig. 22.10 Histology on biopsy taken 2years after grafting of tissue-engineered graft consisting of oral keratinocytes and broblasts. There is the formation of deep rete
ridges as a typical histological sign of gingiva. Light
microscopic picture, magnication ×400
keratinocyte- broblast grafts (collagen sponges
seeded with oral keratinocytes and oral broblasts) (Figs. 22.8b and 22.9b) and xed with
Voco Pac and an acrylic splint for 14days. When
removing the splint, a vulnerable but mostly epithelialized wound surface was visible, but the
collagen sponge had completely disappeared.
Twenty-eight days postoperatively, a complete
epithelization was seen. Six months after vestibuloplasty in the grafted area, a keratinized mucosa
was found. In the clinical follow-up of more than
4years, this area of keratinization was stable in
size (Figs.22.8c and 22.9d). There was only little
shrinkage and an extension of keratinized
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