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J Clin Periodontol 2014; 41 (Suppl. 15): S123S142 doi: 10.1111/jcpe.

12185

The addition of soft tissue umer1 and


Otto Zuhr1,2, Daniel Ba
Markus Hu rzeler1,3
1
rzeler/Zuhr, Munich,
Private Practice Hu

replacement grafts in plastic Germany; 2Department of Periodontology,


Centre for Dental, Oral, and Maxillofacial
Medicine (Carolinum), Johann Wolfgang

periodontal and implant surgery: Goethe-University Frankfurt/Main, Frankfurt,


Germany; 3Department of Operative Dentistry
and Periodontology, University Dental

critical elements in design and


School, University of Freiburg, Freiburg,
Germany

execution
Zuhr O, B aumer D, H urzeler M. The addition of soft tissue replacement grafts in
plastic periodontal and implant surgery: critical elements in design and execution. J
Clin Periodontol 2014; 41 (Suppl. 15): S123S142. doi: 10.1111/jcpe.12185.

Abstract
Soft tissue replacement grafts have become a substantial element to increase tissue
volume in plastic periodontal and implant surgery. Autogenous subepithelial con-
nective tissue grafts are increasingly applied in aesthetic indications like soft tissue
thickening, recession treatment, ridge preservation, soft tissue ridge augmentation
and papilla re-construction. For the clinical performance of connective tissue
graft harvesting and transplantation, a fundamental understanding of the anat-
omy at the donor sites and a sound knowledge of tissue integration and re-vascu-
larization processes are required. Possible donor sites are the anterior and
posterior palate including the maxillary tuberosity, providing grafts of distinct
geometric shape and histologic composition. The selective clinical application of
different grafts depends on the amount of required tissue, the indication and the
personal preference of the treating surgeon. One of the main future challenges is
to volumetrically evaluate and compare the efficacy and long-term stability of soft
tissue autografts and their prospective substitutes. The aim of this review was to
Key words: donor sites; graft harvesting; soft
discuss the advantages and shortfalls of different donor sites, substitute materials
tissue augmentation; soft tissue replacement
and harvesting techniques. Although standardized recommendations regarding graft; soft tissue substitute; subepithelial
treatment choice and execution can hardly be given, guidelines for predictable connective tissue graft
and successful treatment outcomes are provided based on clinical experience and
the available scientific data. Accepted for publication 16 October 2013

The use of soft tissue replacement soft tissue autografts has character- on the belief that a minimal width of
grafts has become a substantial ele- ized the last 50 years of clinical peri- keratinized gingiva would be
ment in plastic periodontal and odontology, and till today more required to maintain the periodontal
implant surgery. The application of than ever a variety of soft tissue tissues healthy and stable (Nabers
grafting interventions is carried out 1954, Ochsenbein 1960, Friedman &
Conflict of interest and source of with two different targets being pur- Levine 1964, Sullivan & Atkins
funding statement sued: increasing the width of kerati- 1969, Carranza & Carraro 1970,
nized tissue and increasing soft tissue Hall 1981, Matter 1982). A mini-
The authors declare that they have no
volume. In the beginning of the era mum of 1 mm to 3 mm of kerati-
conflict of interest. This review article
has been self-funded by the authors.
of mucogingival surgery, surgical nized gingiva was believed to be
interventions were performed based mandatory (Corn 1962, Bowers
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd S123
S124 Zuhr et al.

1963, Lang & Loe 1972). In the thetic indications. In search of better ing soft tissue grafting techniques
1960s, it was assumed that the tissue alternatives it soon became clear that in plastic periodontal and implant
around teeth adapts to functional the predictability regarding the aes- surgery and to provide clinical
requirements when subjected to thetic outcome was much higher strategies for soft tissue replacement
physical impacts during mastication when using a subepithelial connec- graft procedures. Based on scientific
(Ivancie 1957, Orban 1957, Bradley tive tissue graft (SCTG) (Langer & evidence and clinical experience it
et al. 1959, Pfeifer 1963). As a conse- Calagna 1980, Langer & Langer is supposed to (I) analyse and dis-
quence, denudation techniques (Och- 1985, Raetzke 1985, Nelson 1987, cuss the advantages and shortfalls
senbein 1960, Bohannan 1962, Corn Harris 1992, Allen 1994, Bruno of different donor sites and har-
1962, Wilderman 1964), periosteal 1994). The further development of vesting techniques as related to
retention procedures (Staffileno et al. soft tissue autografts from the FGG autogenous soft tissue grafts and
1962) and apical repositioned flaps to the SCTG represents a paradigm (II) to provide clinical guidelines
(Friedman 1962) were recommended shift, which is conceptually anchored for predictable and successful treat-
to increase the width of the kerati- in the literature by the transition ment outcomes and (III) give a
nized gingiva. As the role of inherent from classical mucogingival surgery global perspective on current and
factors regarding genetic determina- to plastic periodontal surgery. Today future possibilities with soft tissue
tion of gingival tissues became clear soft tissue augmentation only occa- substitutes.
later on (Karring et al. 1971, 1974, sionally means widening of the gin-
1975), the use of pedicle grafts and giva or peri-implant mucosa in the
Anatomical landmarks
in particular free epithelialized context of plastic periodontal and
grafts, usually referred to as free gin- implant surgery. It is rather indi- The oral mucosa can be divided into
gival grafts (FGG), was proposed cated for soft tissue recession treat- three portions: the specialized sen-
instead (Haggerty 1966, Nabers ment at teeth (Cairo et al. 2008, sory mucosa (taste buds on dorsum
1966, Sullivan & Atkins 1968, Edel Chambrone et al. 2010, 2012, Cortel- of the tongue), the lining mucosa
1974). lini & Pini Prato 2012) or implants (lips, cheeks, vestibule, floor of the
When it was subsequently real- (Burkhardt et al. 2008, Roccuzzo mouth, base of the tongue and soft
ized that the biological significance et al. 2013, Zucchelli et al. 2013), for palate) and the masticatory mucosa
of a sufficient wide keratinized gin- ridge preservation procedures with (gingiva and hard palate) (Orban &
giva was doubtlessly overrated in the immediate implants or fixed partial Sicher 1945). The masticatory
past (Miyasato et al. 1977, Hangor- dentures (Esposito et al. 2012, Lang mucosa of the hard palate is com-
sky & Bissada 1980, Lindhe & et al. 2012), for soft tissue ridge aug- posed of three histologic layers: the
Nyman 1980, de Trey & Bernimou- mentation associated with implants epithelium, and the subepithelial
lin 1980, Dorfman et al. 1982, Schoo or fixed partial dentures (Thoma connective tissue with the lamina
& van der Velden 1985, Kisch et al. et al. 2009, Schneider et al. 2011, propria and the submucosa (Fig. 1).
1986, Salkin et al. 1987), the clinical Sanz et al. 2012) and for papilla The epithelium is characterized by
importance of FGGs to increase the reconstruction (Nemcovsky 2001, orthokeratinization and about
width of the keratinized gingiva Nordland et al. 2008). Furthermore, 300 lm thick, its structure basically
more and more decreased. Instead it might be recommended for soft corresponding to that of the gingival
periodontists started to use the FGG tissue thickening to stabilize the gin- epithelium. The lamina propria
for aesthetic corrections like soft tis- giva, for example. before orthodon- below the palatal epithelium is very
sue recession coverage (Bernimoulin tic (Steiner et al. 1981, Wennstrom coarse tissue. It contains a high pro-
et al. 1975, Miller 1982) and soft tis- et al. 1987) or restorative (Ericsson portion of inter-cellular substance,
sue ridge augmentation (Seibert & Lindhe 1984) treatment and to which is produced by fibroblasts.
1983) as well as for socket preserva- mask discoloured roots or shining This extracellular matrix is responsi-
tion in aesthetically relevant areas through implant components (Jung
(Landsberg & Bichacho 1994). These et al. 2007).
advancements of soft tissue augmen- Considering the challenges of
tation procedures were marked by a soft tissue augmentation procedures
sense of aesthetics among patients, in plastic periodontal and implant
which had not been present in the surgery today, the FGG has conse-
dental community in this form quently disappeared from the aes-
before. This meant a fundamental thetic zone and its scope of
change regarding the indications of application has been limited to pro-
soft tissue autografts in periodontol- cedures increasing the keratinized
ogy. However, as much as the FGG tissue around teeth and implants in
had proven for increase in the width aesthetically irrelevant zones. For
of keratinized gingiva, as much its that reason, this review dispenses
Fig. 1. Clinical view of a thick free epi-
limitations, both regarding the quan- FGGs and concentrates on SCTGs
thelialized graft without periosteum har-
titative (volume augmentation) and and their potential substitutes for vested from the lateral palate to illustrate
qualitative outcomes (aesthetic inte- soft tissue recession treatment and the histological composition of the pala-
gration, surface, colour, scarring), soft tissue volume increase. The tal masticatory mucosa: covering epithe-
were obvious when it was applied aim of this review was therefore to lium and subepithelial connective tissue
for soft tissue re-construction in aes- analyse the dental literature regard- including lamina propria and submucosa.
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Soft tissue replacement grafts S125

ble for the mechanical properties of age (Song et al. 2008). Furthermore, sek and Rungruang found that the
the tissue layer. It consists predomi- there was a tendency for an increase GPF was most frequently found in
nantly of collagen fibrils mainly with from the canine to the second pre- the region near the apices of the
type I and II and few type V and VI molar, a decrease at the first molar second and third molars, in the area
collagen. Elastic fibres are hardly and an increase again at the second where the vertical and horizontal
present. The lamina propria is molar. The second pre-molar region segments of the palatine bone come
divided into the papillary portion showed to be thickest with a mean together (Klosek & Rungruang
and the reticular portion. The papil- of 3.81  0.75 mm and the first 2009). Ikuta and coworkers found
lary portion shows finger-like projec- molar region the thinnest with in a cone beam computed tomogra-
tions that inter-lock with the 3.13  0.69 mm. In a cadaver study phy study that the GPF was located
overlying epithelium whereas the by Gapski and coworkers, the soft in 92 of 100 cases in the third molar
reticular portion consists of thick tissue thickness at the tuberosity region and in an average distance of
and dense reticular fibres. The sub- came out to be 2.54 mm (Gapski 7.9 mm from the alveolar ridge (Ik-
mucosa is a connective tissue layer, et al. 2006). Apparently, the subepi- uta et al. 2013), whereas a study in
which attaches the lamina propria to thelial connective tissue from the Indian skulls observed the GPF to
the periosteum of the underlying tuberosity area is a very dense, be in the third molar region in only
bone. Numerous glands, nerves and coarse and collagen-rich tissue that 73% of the cases (Sharma & Garud
adipose tissue are present in this tis- seems to contain less fat and glandu- 2013). Monnet-Corti and coworkers,
sue layer. Its thickness can vary lar tissue, but much more collagen who measured the distance of the
between patients and within the than that from the anterior lateral main branches of the GPA from the
same individual (Muller et al. 2000). palate. palatal gingival margin in 198 plas-
The submucosa is characterized by a The arterial blood supply of the ter models of periodontally healthy
rather fatty zone in the anterior and palate is provided by the greater pal- patients, found that the average dis-
copious glands (Gll. Palatinae) in the atine artery (GPA), a branch of the tance from the gingival margin to
posterior area whereas it is in gen- maxillary artery, which emerges the GPA ranged from approxi-
eral less pronounced in the posterior from the greater palatine foramen. It mately 12 mm in the canine area to
than in the anterior part of the pal- runs through a groove lateral to the roughly 14 mm at the second molar
ate. In a histologic evaluation of greater palatine nerve (GPN) and level (Monnet-Corti et al. 2006).
human SCTGs from the anterior submits branches to the palatal The authors concluded that it
palate by Harris, large differences in mucosa and the gingiva, continu- should be possible to harvest a
the histologic composition were ously decreasing its diameter and SCTG measuring 5 mm in height in
found: some grafts consisted almost ends at the incisive canal, where it all patients and 8 mm in height in
only of lamina propria and in some anastomoses with the sphenopalatine 93% of patients without a risk of
grafts the greatest proportion was artery. The innervation of the damaging the GPA. However, a
submucosa with mainly adipose tis- mucosa and gingiva at the hard pal- cadaver study by Fu and coworkers
sue (Harris 2003). The portion of the ate is provided by the GPN, which revealed that the predicted location
lamina propria varied between 21.1 emerges also through the greater pal- of the GPA based on the aforemen-
and 100% of the graft (mean atine foramen and traverses medial tioned study cast measurements
65.2%). These results confirm the to the GPA, subdividing into several tended to be inaccurate and that the
clinical observation that the dimen- branches, which are becoming thin- predicted distance between the GPA
sions of the different subepithelial ner towards the epithelial layer. and the cementoenamel junction of
connective tissue layers vary substan- Between the GPA and the GPN, a the first molars and pre-molars
tially from patient to patient. crest is present, which can in most tended to be underestimated (Fu
The thickness of the masticatory cases be palpated clinically (Bennin- et al. 2011). This is in correspon-
mucosa at the palate has been evalu- ger et al. 2012). dence to findings by Benninger and
ated in different studies. Eger and With respect to potential compli- coworkers, who measured an aver-
M uller determined the thickness with cations of harvesting SCTGs from age distance of 12 mm (range 9
ultrasonic devices (Eger et al. 1996, the palate, the palatine neurovascu- 16 mm) between the first molar and
Muller et al. 2000). They found that lar bundle is a very important and the GPA (Benninger et al. 2012). To
the soft tissue thickness at the tuber- clinically relevant anatomical struc- establish a guideline for clinicians to
osity area was highest with more ture to be protected. Therefore, hav- localize the GPA, the authors
than 4 mm, followed by the palatal ing a general idea of the possible assumed that in most cases the
masticatory mucosa at the second course of the palatine artery is GPA would be found at a distance
molars and pre-molars with an aver- essential. For this reason, different of 76% of the palatal height mea-
age of 3 mm. In general, the thick- anatomical studies were set up with suring from the cementoenamel
ness was found to be higher in men the objective to work out reliable junction of the first molar. Other
than in women. In a computertomo- reference points and guidelines that evidence suggests that the height of
graphic study by Song and cowork- can be used by clinicians to prevent the palatal vault is related to the
ers, it was found to be damage to the GPA during SCTG course of the greater palatine artery:
3.83  0.58 mm with females having harvesting in a given clinical situa- The shallower the palatal vault, the
a thinner (3.66  0.52 mm) mucosa tion. In an anatomical study of the closer the palatine artery gets to the
than men (3.95  0.60 mm) and an GPA and related bony structures of palatal gingival margin (Reiser et al.
increasing thickness with increasing the hard palate in 41 cadavers, Klo- 1996) (Fig. 2).
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
S126 Zuhr et al.

lar ridge augmentation is rather per- as good with the requirements for
formed with a voluminous graft from graft survival in the course of plas-
the tuberosity area whereas a reces- matic circulation and re-vasculariza-
sion coverage can also be done with a tion during the early postoperative
thin and small dimensioned graft phase. As a clinical consequence
from the posterior lateral palate. SCTGs from the posterior palate
Should the clinical situation require seem in contrast to SCTGs from
changing the geometry of a given the anterior area to need being
graft, the transplant can be modified fully covered by a flap to ensure
by folding and suturing grafts from healing by primary intention. It is
the lateral palate or by slicing and presently unclear to what extent it
unfolding grafts from the tuberosity might play an additional role in this
area. As the dimensions of the masti- context if, depending on the
catory mucosa at the palate vary sub- employed harvesting technique, the
stantially from patient to patient periosteum covering the palatal bone
(Eger et al. 1996, Muller et al. 2000, is included in the graft or not.
Harris 2003, Gapski et al. 2006, Song SCTGs can also be harvested
et al. 2008), it is important for the cli- from the palate with covering epithe-
nician to quickly overview the lium according to FGGs, provided
Fig. 2. The blood vessels that supply the
amount of available tissue at the pos- that they are deepithelialized extrao-
lateral palate region can be seen in this
anatomical specimen. The greater pala- sible donor sites. To do so, a good rally. This approach has the advan-
tine artery emerges from the greater pala- and simple option is using an end- tage that SCTGs can also be taken
tine foramen and extends along the odontic needle with a silicon disc in situations with a very thin masti-
lateral palate in an anterior direction. applied to it (Studer et al. 1997, Pao- catory mucosa and that the graft
Due to its size, injury to the greater pala- lantonio et al. 2002, da Silva et al. preparation itself can be performed
tine artery, particularly in its distal seg- 2004, Joly et al. 2007). In this con- more superficially, thereby not vio-
ment, can be expected to result in text, Zucchelli and coworkers lating blood vessels and nerve fibres
massive bleeding. It is therefore crucial to assumed that in addition to measur- running in deeper layers. In this
take precautions to prevent damage to ing soft tissue thickness at the palate way, transplants with more extensive
the artery when subepithelial connective
tissue grafts are harvested from the
endodontic needles might also be surfaces can be gained in a short
palate. used to estimate the composition of amount of time and the allegedly
the subepithelial connective tissue. high-quality tissue layer of the lam-
The authors believed that due to dif- ina propria can be used to full
ferent penetration resistances towards extent as no parts of it remain in the
the needle the transition between lam- flap at the donor site like in under-
Donor site selection
ina propria and the adipose submu- mining harvesting techniques. On
It is beyond all question that among cosa could be felt in many situations the other hand, this procedure might
suitable donor sites for intra-oral (Zucchelli et al. 2010). adversely affect patient morbidity:
SCTG harvesting only those come Besides their geometry, grafts In several clinical studies it could be
into consideration that promise an from different donor sites vary in demonstrated that a more painful
adequate amount of obtainable tis- their histologic composition (Harris post-operative course could be
sue. They should not be associated 2003). It may be speculated that observed in FGG patients with a
with major health risks and go along these differences not only account palatal wound healing by secondary
with acceptable patient morbidity. for variable volume stability but also intention in contrast to SCTG
Under these requirements and in influence the physiologic process of patients where a flap was raised, the
consequence of the anatomical soft graft re-vascularization. From clini- graft harvested internally and the
tissue conditions in the oral cavity cal experience, it seems in this con- wound allowed to heal by primary
two areas of interest for autograft text as if subepithelial connective intention (Farnoush 1978, Jahnke
harvesting have emerged as the areas tissue from the tuberosity and the et al. 1993, Del Pizzo et al. 2002,
of choice: the anterior and the posterior lateral palate was denser Griffin et al. 2006, Wessel & Tatakis
posterior palate, whereas in the pos- and firmer than that from the ante- 2008). However, these results are
terior area the tuberosity and the lat- rior palate. It can be assumed that it contrary to a recent clinical study
eral palate can be distinguished. is therefore less susceptible to post- identifying influencing factors for
In general, the grafts from the dif- operative shrinkage. On the other pain sensation after FGG removal
ferent eligible sites differ in their geo- hand, this very dense and coarse (Burkhardt et al. in preparation)
metric shape: grafts from the connective tissue appears to undergo and a randomized controlled clinical
tuberosity are more voluminous, necrosis more easily than that from trial (RCT) comparing patient mor-
those from the posterior lateral palate the anterior palate. It may be bidity after FGG and SCTG har-
rather thin, whereas those from the hypothesized that compared to the vesting procedures (Zucchelli et al.
anterior palate can often be extensive rather loose formation of the subepi- 2010). In both studies it could be
with a large surface. This has an influ- thelial connective tissue from the demonstrated that post-operative
ence on the indication they are anterior palate, the dense tissue from pain was rather influenced by the
intended for. For example, an alveo- the posterior area does not comply thickness of the graft and the
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Soft tissue replacement grafts S127

remaining soft tissue at the palate, from different donor sites seem to basically in the particular position
but by primary or secondary wound have different characteristics that of the donor site, the number and
healing at the donor site. It can be might require selective clinical appli- type of surface incisions and in the
mentioned as an aside that in the cation and well thought out surgical flap design for gaining access to the
latter study, the deepithelialized protocols. The clinical decision graft. In principle, they can be sub-
autografts consisting of lamina pro- where to harvest soft tissue auto- divided into techniques that provide
pria only led to a statistically signifi- grafts from is presently hardly based SCTGs with or without a remaining
cant higher increase in buccal on written evidence, but rather relies collar of keratinized epithelium.
gingival thickness following reces- on clinical experience and depends Relating to the group of SCTGs
sion coverage (Zucchelli et al. 2010). on the amount of available tissue at with epithelium, Langer and Cala-
These findings support the afore- the eligible donor sites, the indica- gna as well as Langer and Langer
mentioned clinical observation that tion in which the transplant is sup- introduced a harvesting method
SCTGs containing presumed denser posed to be used and last, but not based on a rectangular incision
subepithelial connective tissue are least on the personal preference of design with two horizontal and two
comparatively less prone to postop- the treating surgeon. vertical incisions resulting in SCTGs
erative shrinkage. The clinical expe-
rience that using SCTGs that are
harvested with epithelium and deepi-
thelialized outside the oral cavity
seem to bear an increased risk for
postoperative scar tissue formation
at the recipient site should not be
neglected, though. At this point of
time any attempted explanation
would be speculative in nature,
although it would be possible that in
(a) (b)
contrast to SCTGs from deep sub-
epithelial connective tissue zones
SCTGs consisting mainly of a super-
ficial layer of subepithelial connec-
tive tissue behave more similar to
FGGs with all the negative conse-
quences for the qualitative treatment
outcomes outlined above (aesthetic
integration, surface, colour, scar-
ring). This might potentially be
caused by isolated fragments of epi- (c) (d)
thelium that are left in the graft
Fig. 3. Clinical view of soft tissue grafts harvested from the different possible donor
after deepithelialization, especially
sites with varying geometric shape and histologic composition: from the anterior lat-
due to the papillary inter-locking eral palate (a), from the posterior lateral palate (b), from the lateral palate, deepitheli-
between the epithelium and the lam- alized extraorally (c) and from the maxillary tuberosity (d).
ina propria. In a study by Harris,
SCTGs were manually deepithelial-
ized at the best optical control by with an epithelial collar of about
Harvesting techniques
the surgeon (Harris 2003). The 2 mm width (Langer & Calagna
subsequent histological analysis, The clinical procedure of SCTG har- 1980, 1982, Langer & Langer 1985).
though, could demonstrate remain- vesting from the palate is often char- Subsequently, Harris used a very
ing epithelium in 80% of the grafts. acterized by the remarkable similar approach and modified the
In addition, more aggressive mor- challenge of obtaining the largest technique by limiting the vertical
phogenetic stimuli regarding the dif- volume of tissue possible on one side incisions to a minimal dimension,
ferentiation of the covering while minimizing post-operative pain barely enough to get access to the
epithelium at the recipient site could and reducing the risk of complica- underlying donor tissue (Harris
be suspected in more superficial lay- tions on the other side. To meet 1992). Raetzke, finally, abstained
ers of subepithelial connective tissue these requirements, various proce- from vertical incisions completely
(Ouhayoun et al. 1988). If it would dures for soft tissue autograft har- and used two converging horizontal
make a difference for this reason to vesting in plastic periodontal and crescent-shaped incisions resulting in
position the superficial side of the implant surgery have been developed a wedge-shaped SCTG with an epi-
graft inwards or outwards in the and described in the literature: thelial collar (Raetzke 1985). How-
recipient bed could be an interesting ever, the disadvantage of all these
field of future research (Fig. 3). techniques obtaining SCTGs includ-
SCTG harvesting from the lateral palate
In summary, it can be stated that ing parts of the epithelium was
although the actual reasons are The different SCTG harvesting tech- beside the aforementioned negative
largely unknown up to date grafts niques from the lateral palate vary consequences for the qualitative-aes-
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
S128 Zuhr et al.

thetic treatment outcomes that the given in two recently published text- face instead of on bone or perios-
donor site could not be completely books (Zuhr & H urzeler 2012, Zuc- teum after surgery, which might
covered with the flap and was there- chelli 2013). improve the predictability to achieve
fore partially healing by secondary healing by primary intention.
intention. Due to the rigidity of the SCTG harvesting from the anterior palate
Depending on the clinical indication
palatal masticatory mucosa this and how much tissue is available,
could only be avoided if SCTGs The procedure starts according to SCTGs can be obtained with or
were harvested without epithelium. the single-incision technique with a without periosteum. Grafts with
In consequence, Edel introduced a horizontal incision along the row of periosteum are harvested by blunt
trap-door approach without remov- teeth starting from the mesial border dissection using a periosteal elevator.
ing epithelium from the donor site of the first molar to the lateral inci- For graft removal without perios-
(Edel 1974). By undertaking one sor, 2.0 mm apical to the gingival teum, an additional offset incision is
horizontal and two vertical inci- margin, 1.01.5 mm deep. All the carried out above the periosteum by
sions, an access flap could be remaining incisions are undermining sharp dissection with a scalpel blade.
raised, the graft removed and com- below the mucosal surface. With Although leaving periosteum on the
plete wound closure achieved. How- regard to post-operative pain, it bone has probably positive conse-
ever, particularly in cases with seems to be the main challenge from quences in terms of post-operative
unfavourable relations between flap a surgical point of view to achieve wound healing, clinical experience
base and pedicle length flap slough- primary wound healing at the palatal has shown that SCTGs with perios-
ing could be observed causing donor site. In this context, it appears teum have superior mechanical sta-
unnecessary discomfort for the to be essential to guarantee an ade- bility, which might be an advantage
patient (Edel 1974, Harris 1994, quate postoperative blood supply for relating to the clinical handling of
1997). This is why H urzeler and the access flap and therefore prepare those grafts in certain situations. For
Weng proposed a single-incision a partial-thickness flap of uniform the following wound closure parallel
technique for SCTG harvesting thickness and proper dimension. For and crossed horizontal sling sutures
from the lateral palate later on this reason, it is mandatory to per- are recommended. The placement of
(Hurzeler & Weng 1999). The exe- form the initial horizontal incision this type of sutures around the max-
cution of only one horizontal sur- with a scalpel held strictly perpendic- illary posterior teeth has a wound
face incision followed by an ular to the palatal surface. To ensure compressing effect that might be
undermining flap preparation that the following split-thickness flap beneficial particularly in terms of
seemed to positively affect post- preparation will provide a flap of promoting hemostasis and primary
operative healing and patient mor- sufficient dimension throughout, it is adaptation of the wound margins
bidity compared with the trap-door important to gradually increase the (Zuhr & H urzeler 2012) (Fig. 4).
technique (Del Pizzo et al. 2002, angle of the blade until it is parallel
Wessel & Tatakis 2008). In the fol- to the palatal surface by making
SCTG harvesting from the posterior
lowing, three distinct and obviously repeated distal to mesial movements, lateral palate
frequently applied techniques to mainly with the tip of the scalpel.
harvest SCTGs from the lateral pal- Care must be taken to ensure that The harvesting procedure is carried
ate will be proposed: SCTG har- the flap preparation is not substan- out at the first and second maxillary
vesting from the anterior palate, tially extended more than 10 mm molars and usually contains one hor-
SCTG harvesting from the posterior apical from the cementoenamel junc- izontal and two vertical incisions
lateral palate and SCTG harvesting tion of the maxillary posterior teeth. according to the trap-door approach.
from the lateral palate by obtaining If placed roughly 2 mm from the ce- Depending on the soft tissue thick-
a graft with epithelium correspond- mentoenamel junction, the initial ness at the donor site and the size of
ing to a FGG that is deepithelial- incision can be safely extended api- the graft to be harvested one or in
ized extraorally. In this respect cally to a depth of approximately individual cases even both vertical
ideally those surgical protocols 8 mm without a risk of damaging incisions can be omitted. While the
should be picked out that have sci- the great palatine artery. As the cut- horizontal incision is performed 1
entifically proven to be the presently ting portion of a No. 15 scalpel 2 mm apical of the gingival margin,
best possible treatment options. blade is approximately 8 mm in the two vertical incisions should
However, at the time being it is in length, it can serve as a gauge for extend 1 mm further than the
this context hardly possible to safe graft harvesting on this occa- intended apicocoronal dimension of
choose one approach over the other sion. After that the size of the graft the graft offering access to the apical
one based on scientific evidence. is defined by executing two horizon- incision line in the connective tissue
For this reason, those clinical proce- tal and two vertical incisions inside later on. A split-thickness flap is
dures were selected that seem to the created envelope. They should be then prepared parallel to the external
reflect a contemporary mindset and extended to the bone and overlap at mucosal surface by watching the
presently seem to be based upon intersections. It might be advisable blade working from outside under
sound clinical experience if SCTGs to place the coronal internal incision the flap. By doing so, the goal is to
are harvested from the lateral pal- roughly 1.01.5 mm apical to the ini- create a flap of uniform thickness,
ate. The subsequent SCTG harvest- tial horizontal incision. This ensures whereby the releasing incisions can
ing step by step descriptions are that the access flap will rest on a be used as flap thickness guides.
based on clinical recommendations well-perfused connective tissue sur- Now the horizontal incision of the
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Soft tissue replacement grafts S129

sective periodontal surgery. It is eas-


ier to perform if the terminal tooth
is the first molar, but it can also be
accomplished with second or third
molars present. The procedure starts
with two converging incisions per-
pendicular to the tissue surface and
1.01.5 mm deep as far distal to the
last molar as possible while remain-
(a) (b) ing within the masticatory mucosa.
Then, an undermining partial-thick-
ness incision buccal and palatal up
to the mesial surface of the last
molar is made. The scalpel is guided
successively parallel to the buccal or
palatal soft tissue surfaces to yield a
partial-thickness flap of uniform
thickness throughout. After a supra-
periosteal incision is made the
(c) (d) wedge-shaped graft is removed from
the donor site by sharp dissection.
Fig. 4. (a) If the initial incision is placed approximately 2 mm from the gingival mar- The covering epithelium on the
gin of the maxillary posterior teeth, the current scientific evidence suggests that it upper part of the graft is conse-
would be virtually impossible to damage the greater palatine artery or its major quently removed extraorally. The
branches if the subepithelial connective tissue graft is harvested no more than 8 mm donor site is closed with an external
apical to the initial incision line. Because the cutting portion of a No. 15 scalpel blade
horizontal mattress suture anchored
is roughly 8 mm in length, it can serve as a gauge for safe graft harvesting. (b) Clinical
experience has shown that it is much easier to achieve primary wound healing if the to the periosteum. Additional single
initial and coronal harvesting incisions are slightly offset to create a small shelf of soft interrupted sutures can be used to
tissue on which the palatal access flap can rest postoperatively. (c) Subepithelial con- completely close the wound (Zuhr &
nective tissue grafts from the anterior lateral palate can be comparatively extensive Hurzeler 2012) (Fig. 7).
and include to some extent fatty tissue. (d) Postoperative situation after wound closure Independently of the selected
by application of parallel and crossed horizontal sling sutures. donor site and the applied SCTG
harvesting technique, it takes a cer-
tain amount of time from the
graft is made along the horizontal perpendicular to the mucosal surface, moment when the graft is taken
incision of the flap perpendicular to 1.01.5 mm deep. Now the blade is from the palate until the wound at
the underlying bone and the mesial rotated to be almost parallel to the the palatal donor site is closed. In
and distal internal incisions are mucosal surface and moved apically the meantime care should be taken
done. Consequently, the blade is as far as a FGG of uniform thickness to prevent graft dehydration, for
rotated to be parallel to the external is mobilized being 0.5 mm thicker example by storing the SCTG in
surface and a second undermining than actually needed. Subsequently, gauze soaked in physiologic saline
incision with the scalpel is performed compressive sling sutures anchored to until further use. Extraoral modifica-
attempting to maintain uniform graft the soft tissue apical to the palatal tion in SCTGs is often necessary. A
dimensions in the aspired graft wound area are applied. The graft is proven way to do this is to first
thickness. Then the connective tissue then positioned on sterile gauze, spread and press the graft on a wet
is freed apicocoronally and mesiodis- moistened with a saline solution and glass slab using a surgical forceps. A
tally before making the apical inci- deepithelialized with a sharp scalpel fresh scalpel blade is then applied to
sion almost perpendicular to the blade held parallel to the external cut the graft to the desired size and
bone surface to completely detach graft surface. To distinguish between shape and to thin the SCTG as
the SCTG. At the end, single inter- epithelium und subepithelial connec- needed. Due to the possibility to act
rupted sutures can be used to pri- tive tissue and therefore make sure as a barrier to plasmatic circulation
marily adapt the wound margins and that the epithelium is completely and re-vascularization during the
therefore provide the donor site for removed from the graft the use of early phase of healing fat and glan-
healing by primary intention (Zucch- magnification aids is recommended dular tissue remnants detected on
elli 2013) (Fig. 5). (Zucchelli 2013) (Fig. 6). the graft should be removed (Sulli-
van & Atkins 1968).
The routine use of surgical stents
SCTG harvesting from the lateral palate SCTG harvesting from the maxillary
tuberosity
after harvesting SCTGs from the lat-
with a FGG that is deepithelialized
extraorally
eral palate is recommended for many
Technically, the clinical procedure reasons. First, the stent applies pres-
At first, two horizontal and two verti- for harvesting SCTGs from the max- sure to the wound, which seems to
cal incisions are performed according illary tuberosity corresponds to that promote post-operative flap adapta-
to the size of the area to be grafted, for the distal wedge technique in re- tion and wound healing. Second, the
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
S130 Zuhr et al.

site from mechanical irritation but


also seems to enhance patient com-
fort considerably during the first
postoperative days. The results of a
RCT by Thoma and coworkers indi-
cate that the application of a colla-
gen matrix at the palatal wound
might additionally enhance soft tis-
sue healing and re-epithelization at
(a) (b) early time points if an extraorally
deepithelialized FGG was harvested
(Thoma et al. 2012). The use of a
surgical stent is not required after
SCTG harvesting from the maxillary
tuberosity.
The amount of tissue needed for
defect re-construction is potentially
greater than the amount of tissue
available, even if harvested from
(c) (d) both sides of the palate. Therefore,
it is sometimes necessary to harvest
Fig. 5. (a) The harvesting procedure at the posterior lateral palate equals a trap-door subepithelial connective tissue from
approach: it usually contains one horizontal and two vertical incisions. (b) A split- the palate at two different times.
thickness flap is then prepared parallel to the external mucosal surface creating a flap Harris and coworkers could demon-
of uniform thickness, whereby the releasing incisions can be used as flap thickness strate that this approach causes no
guides. (c) Subepithelial connective tissue grafts from the posterior lateral palate are significant problems if the second
limited in size compared to those from the anterior palate, but are suggestive to con- procedure is performed after a 2- to
tain less fatty tissue. (d) Horizontal sling sutures can be used to compress the wound
3-month interval (Harris et al. 2007).
area and adapt the flap margins as good as possible.

Tissue integration and volume


stability
In contrary to vascular or pedicle
grafts, free grafts are avascular and
have no direct blood supply. There-
fore, the survival of vital, tissue-spe-
cific cells in a free autologous graft
depends on an early and adequate
blood supply from the recipient bed
(a) (b)
and the overlying flap by means of
plasmatic circulation and, later on,
by means of re-vascularization of the
graft.
The healing of FGGs has been
studied in a variety of animal experi-
ments (Oliver et al. 1968, Jansen
et al. 1969, Nobuto 1986, 1987,
Nobuto et al. 1988). It can be
assumed that their results regarding
(c) (d) the basic concepts of soft tissue
autograft integration can at least
Fig. 6. (a) Two horizontal and two vertical incisions are performed according to the principally be transferred to the
size of the area to be grafted, perpendicular to the mucosal surface, 1.0 to 1.5 mm healing process of SCTGs: During
deep. Then the blade is rotated in order to be almost parallel to the mucosal surface the initial phase of healing, the
and moved apically. (b) A free gingival graft of uniform thickness is mobilized being grafted tissue survives exclusively by
0.5 mm thicker than actually needed. c The graft is then positioned on a sterile glass
plate, moistened with a saline solution and deepithelialized with a sharp scalpel blade
avascular plasmatic circulation from
held parallel to the external graft surface. To distinguish between epithelium und sub- the recipient bed. Apart from their
epithelial connective tissue and therefore make sure that the epithelium is completely limited intra-cellular energy
removed from the graft the use of magnification aids is recommended. (d) The donor resources, the grafts are entirely
site is left for healing by secondary intention. dependent on the influx of oxygen
and metabolites within the extracel-
stent enables a rapid and effective operative bleeding. Third, the stent lular fluid, the driving force behind
response to intra-operative or post- not only protects the palatal donor this diffusion process being the con-
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Soft tissue replacement grafts S131

cannot be detected anymore (Gargi-


ulo & Arrocha 1967). The results of
the above-quoted animal experi-
ments could partially be confirmed
in a clinical study by M
ormann and
coworkers (Mormann et al. 1975).
Under the use of fluorescein angiog-
raphy, the post-operative diffusion
and re-establishment of capillary
(a) (b) blood circulation could be investi-
gated. The authors observed the for-
mation of capillary loops between
the seventh and 14th post-operative
day and concluded that blood circu-
lation in FGGs is re-established pri-
marily by capillary budding.

Wound healing and clinical outcomes in


avascular beds
(c) (d)
When using SCTGs to cover soft tis-
Fig. 7. (a) Two converging incisions are made with a No. 15 scalpel blade. They sue recessions at teeth or implants,
should start at the distal surface of the last molar and extend as far distally as possible part of the recipient site will be the
while remaining in the masticatory mucosa. The incisions should be made perpendicu- avascular root or implant surface.
lar to the surface to a depth of approximately 1.0 to 1.5 mm. To harvest as large a Consequently, graft survival depends
volume of tissue as possible, the incisions should include all of the soft tissue around on a sufficient blood supply originat-
the distal tooth surface. (b) After a supraperiosteal incision was made, the graft is ing from the vascular recipient bed
removed from the donor site by sharp dissection. (c) The wedge-shaped connective tis- adjacent to the recession defect and
sue graft immediately after harvesting. To prevent dehydration, the graft should be
the covering flap (Fig. 8). In an
stored in gauze soaked in physiologic saline until further use. (d) The donor site is
closed with a crossed periosteal suture. Anchorage of the suture in this manner (by the experimental study by Guiha and
periosteum buccally and by the masticatory mucosa palatally) serves two purposes: coworkers, artificially created gingi-
apical flap repositioning and wound compression. Interrupted sutures can be used to val recessions were treated under the
close the remaining wound areas in the distal region. use of SCTGs harvested from the
palate (Guiha et al. 2001). Histologi-
centration gradient between the izontal anastomoses can be cal evaluation was performed at 7,
native and the transplanted tissues. observed. Capillary budding takes 14, 28 and 60 days after surgery
The thinner the initially formed exu- place throughout the graft and a demonstrating re-vascularization of
date between bed and graft and the fibrous union with the graft bed is the grafts by capillary proliferation
more immobile the graft is, the eas- established. Capillaries proliferate originating from the periodontal
ier plasmatic circulation can occur and re-build a dense vascular net- plexus, the supraperiosteal plexus
and the more living cells can survive. work extending beyond the pre-exist- and the overlying flap. The trans-
From the third to fourth post-opera- ing graft margins. Simultaneous to planted tissues seemed to be vascu-
tive day on the re-vascularization the re-vascularization process, exfoli- larized completely after 14 days and
phase begins. During this time, Nob- ation of the epithelium on the graft after 28 and 60 days demarcation
uto and coworkers observed a medi- can be observed and re-epithelializa- zones between graft and flap or peri-
ator-stimulated ingrowth of tion occurs mainly by proliferation osteum could not be identified any-
capillaries from the wound bed into of epithelium from the adjacent tis- more. In contrary, a few 2-week
the graft and the formation of anas- sues, indicating that the survival of specimens showed a bigger dimen-
tomoses between blood vessels of the the graft depends on the trans- sioned blood clot at the interface
recipient bed and the transplanted planted connective tissue layer only. between graft and recipient bed and/
tissues the blood circulation is Subsequent to the re-vascularization or graft and flap obviously not
reestablished by reusing the pre- phase, from the 11th post-operative allowing blood vessels to penetrate
existing vascular network of the day on, the maturation phase sets in. to the graft. The authors assumed
graft (Nobuto 1986, 1987, Nobuto At this point of time, the amount of the re-vascularization and healing
et al. 1988). After the fifth post- blood vessels is gradually reduced to process to have been delayed in these
operative day, the vessels increase a number that is usually found in areas presumably due to a less than
their continuity and form a vascular the oral mucosa, whereas the epithe- optimal adaptation of the graft to
layer in the graftbed junction, a lium simultaneously matures with the recipient bed. Those parts of the
finding that coincides with observa- the formation of a keratin layer. graft not being in contact with the
tions in dye-injected sections by Jan- Only few changes can be observed in root surface and not covered by the
sen and coworkers (Jansen et al. the following time and after about flap were not vascularized at all.
1969). From the seventh day on the 3 weeks the demarcation zones Basically, small areas of SCTGs not
connection of existing vessels by hor- between graft and flap or periosteum completely covered by an overlying
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
S132 Zuhr et al.

that the vascularization of the micro- continuous in vivo monitoring of


surgically treated sites was superior skin graft healing by repetitive intra-
to that of the macrosurgically trea- vital microscopy (Lindenblatt et al.
ted ones immediately after surgery 2008). In an experimental study, the
and after 3 and 7 days post-opera- authors were able to show for the
tively. They could also demonstrate first time a temporary angiogenic
a statistically significant superiority response within the capillaries of the
of the microsurgical technique, based skin graft obviously representing a
on the percentage of root coverage reaction to reperfusion and supply of
one year after treatment. As it can the hypoxic graft with proangiogenic
be assumed that the re-vasculariza- factors (Lindenblatt et al. 2010). In
Fig. 8. When using subepithelial connec-
tive tissue grafts to cover soft tissue
tion process is driven by numerous another animal experiment of the
recessions at teeth or implants, part of signalling pathways, more recent same working group, an early in-
the recipient site will be the avascular research focused on the question to growth of angiogenic wound bed ves-
root or implant surface. Consequently, what extent growth factors might sels into the existing vascular chan-
graft survival depends on a sufficient improve the healing process of nels of the skin graft and subsequent
blood supply originating from the vascu- SCTGs. In a clinical study, Lafzi centripetal replacement of the exist-
lar recipient bed adjacent to the recession and coworkers evaluated the use of ing graft vessels could be indicated
defect and the covering flap. vascular epithelial growth factor in (Calcagni et al. 2011).
conjunction with SCTGs from the Soft tissue healing against a cov-
flap a practice occasionally per- palate for gingival recession treat- ered root or implant surface typi-
formed based on experimental (Kar- ment (Lafzi et al. 2012). In fact they cally results in healthy gingival or
ring et al. 1974) and clinical studies observed better clinical outcomes mucosal conditions without clinical
(Donn 1978, Mackenzie & Fusenig when the growth factors were used, signs of inflammation and pocket
1983, Ouhayoun et al. 1988, Bor- although not statistically significant. formation. Different scientific inves-
ghetti & Louise 1994, Bouchard A study by Jankovic and coworkers tigations studied the quality and nat-
et al. 1994, Cordioli et al. 2001) to comparing platelet-rich membranes ure of the new tissue attachment to
enlarge the width of keratinized tis- with SCTGs for recession treatment previously denuded root surfaces
sue particularly in root coverage observed enhanced wound healing in after a combined therapy with pedi-
procedures though, seem not to the first group with similar treatment cle soft tissue grafts and SCTGs.
entail an increased risk for graft outcomes except for less gain in ker- While only a few experimental stud-
necrosis (Raetzke 1985). In this con- atinized tissue width (Jankovic et al. ies (Weng et al. 1998) and human
text, Yotnuengnit and coworkers 2012). Although Cheung and histologies (Harris 1999, Goldstein
investigated 15 patients scheduled coworkers also found similar out- et al. 2001) could demonstrate a true
for recession treatment (Yotnuengnit come measures for platelet-concen- new connective tissue attachment
et al. 2004) based on the envelope trated grafts (Cheung & Griffin with new cementum, new bone and
technique (Raetzke 1985). They mea- 2004), a RCT by McGuire and inserting PDL fibres in larger quanti-
sured the areas of the SCTGs being coworkers resulted in statistically ties, the majority of scientific evalua-
covered by a flap in relation to the significant recession depth reduction, tions found that only the most
areas left exposed over the originally root coverage and recession width apical and lateral parts of the reces-
denuded root surfaces and identified reduction favouring the SCTG sion defects healed by regeneration
a minimum ratio of 11:1 that should (McGuire et al. 2009a). Two other with new connective tissue attach-
not be substandarded if the goal was studies (Huang et al. 2005, Keceli ment, whereas the main body of the
complete root coverage. The results et al. 2008), in which platelet-rich previously exposed root surfaces
of a clinical investigation by Al-Zah- plasma was added to SCTGs in healed with a long junctional epithe-
rani and coworkers indicated that in recession coverage, found no differ- lium and connective tissue adhesion
this connection the surface orienta- ence in clinical outcomes compared (Harris 1999, Bruno & Bowers 2000,
tion of the SCTG had no significant with SCTGs alone, except for more Guiha et al. 2001, Majzoub et al.
effect on the clinical outcomes of gain of keratinized tissue under the 2001, McGuire & Cochran 2003,
either root coverage or height of ker- implementation of growth factors in Cummings et al. 2005, McGuire
atinized tissue (Al-Zahrani et al. the study by Keceli and coworkers. et al. 2009a,b). High effort was
2004). Burkhardt and Lang assessed Up to date, the knowledge about taken in the past to develop chemical
the outcomes of gingival recession the physiologic proceedings of graft root conditioning agents promoting
coverage using SCTGs in a clinical re-vascularization is mainly based on wound healing outcomes with more
study (Burkhardt & Lang 2005). In histological studies. This has recently new connective tissue attachment.
a split-mouth design, root coverage changed due to the availability of Citric acid, tetracyclin HCL, fibrin
was accomplished by conventional new technologies in combination glue associated with tetracyclin HCL
macrosurgery on one side and by with innovative scientific models to and sodium hypochlorite were used
microsurgery on the other. Fluores- further investigate the healing pro- in combination with scaling and root
cence angiography was performed to cess of free soft tissue autografts. planing to demineralize the root sur-
evaluate the course of healing imme- One promising, forward-looking face and in doing so to expose
diately after surgery and 3 and model was introduced by Lindenblatt the collagen fibres of the dentine
7 days later. The authors could show and coworkers allowing to perform matrix and allow their inter-locking
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Soft tissue replacement grafts S133

with those in the covering connective data from clinical studies could not during the harvesting procedure. In
tissue. However, the results of ani- reveal more pronounced gingival addition, more recessions could be
mal experiments and controlled clini- inflammation and plaque accumula- treated at the same time if necessary
cal trials indicated that chemical tion if class V restorations made of as the required grafts per recession
root surface demineralization cannot different tooth coloured filling mate- could be comparatively small and
improve wound healing outcomes rials were covered with coronally rather thin. Furthermore, the nutri-
and cannot be considered as benefi- advanced pedicle flaps (Lucchesi tional exchange between wound bed,
cial for root coverage procedures et al. 2007, Santamaria et al. 2008). SCTG and covering flap might be
compared to mechanical biofilm Santamaria and coworkers evalu- improved during the early wound
removal only (Roccuzzo et al. 2002, ated in a RCT the treatment of healing period by this type of grafts
Oates et al. 2003, Cortellini & Pini gingival recessions associated with an aspect that might in particular
Prato 2012). Whether the combina- non-carious cervical lesions by play a role if the covering flap is thin
tion of SCTG and root surface SCTGs with a coronally advanced (Hwang & Wang 2006). In this sense
conditioning with ethylenediamine- flap alone or in combination with Zucchelli and coworkers modified
tetraacetic acid before application of the fabrication of resin-modified position, size and thickness of
enamel matrix derivate (EMD) can glass ionomer restorations. Six SCTGs and recommended the use of
influence the type of attachment on months after surgery there was no about 1 mm thick grafts that were
the root surface after gingival reces- statistically significant difference positioned in a distance apical of the
sion treatment is presently unclear between test and control regarding cementoenamel junction that corre-
and needs further scientific verifica- percentage of root coverage. Fur- sponds to the pre-operative width of
tion (Rasperini et al. 2000, Carnio thermore, no clinical signs of keratinized tissue with a mesiodistal
et al. 2002). The clinical observation inflammation could be detected in extension of the recession width plus
of a so-called creeping attachment both groups. The authors credited 6 mm and an apicocoronal dimen-
which refers to a soft tissue matura- the results with the biocompatibility sion calculated as the distance from
tion process with a certain coronal of the filling material, the well fab- the cementoenamel junction to the
migration of the gingival margin at ricated and polished restorations bone crest minus the pre-operative
SCTG-treated sites over time, cannot and the good compliance and oral height of keratinized gingiva. In a
not be explained at present. (Agudio hygiene of the patients (Santamaria RCT using coronally advanced flaps
et al. 2009, Pini Prato et al. 2010). et al. 2009). in combination with SCTGs for
Two clinical case documentations In gingival recession treatment, recession treatment, the authors
reported on external root resorption the combination of coronally compared the conventional type of
after root coverage with SCTGs advanced flaps and SCTGs is pres- graft with the novel approach.
(Hokett et al. 2002, Carnio et al. ently recommended as the treatment Although differences between the
2003). The fact that this is indeed a modality of choice (Cairo et al. two treatment modalities were not
severe but not a common complica- 2008, Chambrone et al. 2012, Cortel- statistically significant regarding per-
tion after gingival recession treat- lini & Pini Prato 2012), whereas on centage of root coverage, aesthetic
ment might be explained by the the other hand uncertainty exists results and patient-centred outcomes
early formation of a root-protective about the real effect of the graft: were superior with the small dimen-
barrier, namely a new connective tis- Cortellini and coworkers compared sioned and apically positioned graft
sue attachment in the most apical in a RCT coronally advanced flaps (Zucchelli et al. 2003). If for any rea-
part and a long junctional epithe- for gingival recession treatment with son the SCTG failed to anchor the
lium in the more coronal part of the and without the additional applica- overlying flap and undesired flap
treated root surfaces. tion of SCTGs (Cortellini et al. retraction occured during the early
It goes without saying that if 2009). The presence of a SCTG wound healing phase the SCTG
instead of natural roots SCTGs are under the flap was associated with a might, on condition that it is posi-
placed against artificial surfaces of reduced soft tissue contraction dur- tioned at the level of the cemento-
implants or restored teeth new con- ing the early phase of healing lead- enamel junction, act as a protector
nective tissue attachment cannot be ing to a significantly greater amount beyond it and still allow healing by
expected. It can be assumed that of sites completely covered at primary intention and successful
the established type of attachment 6 months. These results can be inter- root coverage. This clinical presump-
is slightly different between restored preted in a way that the presence of tion can be supported by the results
tooth and implant and from mate- a SCTG might stabilize the flap in a of a clinical study by Bouchard and
rial to material, and is character- coronal position and therefore serve coworkers comparing coronally
ized by connective tissue adhesion as an anchor for the covering flap advanced and envelope flaps in com-
and primarily by a long junc- during the initial wound healing per- bination with SCTGs for gingival
tional epithelium (Berglundh et al. iod. A variety of clinical conse- recession treatment (Bouchard et al.
1991, Abrahamsson et al. 1998, quences would follow if this 1994). Although treatment outcomes
Gomes et al. 2005, Martins et al. hypothesis was confirmed: SCTG were similar with respect to root
2007). Although subgingival resto- harvesting for gingival recession coverage a significant increase in
ration margins seem to be detri- treatment would be less demanding keratinized tissue height was surpris-
mental to gingival and periodontal for the surgeon in the majority of ingly observed in both groups. These
health over a long period of time the cases and go along with a findings could be expected in the
(Schatzle et al. 2001), short-term decreased risk of damaging the GPA envelope flap group where the most
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
S134 Zuhr et al.

coronal parts of the SCTGs were maintenance of 74% of the aug-


not covered by the flaps, but not in mented volume after 3 months and
the coronally advanced flap group 64% after 12 months respectively.
where instead the overlying flaps With regard to post-operative soft
covered the SCTGs completely tissue volume changes, the healing
(Mackenzie & Fusenig 1983, Ouha- process seemed to be accomplished
youn et al. 1988, Borghetti & Louise after 6 months (Rebele et al. submit-
1994, Cordioli et al. 2001). The ted for publication). With respect to
authors assumed that these results long-term stability after recession
might be caused by a tendency of treatment it can further be specu-
flap retraction during wound healing lated if the SCTG can provide a
Fig. 9. If subepithelial connective tissue
in the coronally advanced flap group positive contribution by thickening grafts are used for soft tissue volume
leaving the most coronal parts of the the marginal soft tissues (Nickles buildups like soft tissue ridge augmenta-
graft uncovered. The fact that et al. 2010, Pini Prato et al. 2010), tions, the prerequisites for uneventful
slightly exposed areas of a SCTG by the long-term effect of a creep- and fast wound healing processes are
usually do not undergo necrosis and ing attachment (Agudio et al. 2009, comparatively favourable as the blood
maintain primary adhesion to the Pini Prato et al. 2010) or by a com- supply for graft integration is provided
root surface might explain the bination of both. Anchoring the by both - the overlying flap and the reci-
observed gain in keratinized tissue overlying flap, protecting healing by pient bed.
height and elucidate the possibly primary intention, increasing mar-
existing protector effect of SCTGs ginal soft tissue thickness or induc- grafting materials. The organic
(Yotnuengnit et al. 2004). Current ing creeping attachment further extracellular matrix could serve as a
scientific investigations seem to fur- progress regarding soft tissue reces- space-holder and the relatively
thermore suggest a positive SCTG sion treatment with combined proce- loosely arranged collagen fibres
effect by increasing marginal soft dures will, to some extent, definitely within the matrix might ensure that
tissue thickness. Zuhr and cowork- be dependent on a better under- plasmatic circulation in the initial
ers compared in a RCT a modified standing of the true SCTG effect. It post-operative period and the subse-
tunnel technique with SCTG from is beyond all doubt that more trans- quent re-vascularization process can
the anterior palate versus a coronally parency in this context will substan- start early and proceed relatively
advanced flap with EMD for root tially influence future research and unimpeded (tissue-conductive char-
coverage (Zuhr et al. accepted for clinical developments. acter). Consequently, the chances
publication). The application of an that a large number of living fibro-
innovative three-dimensional mea- blasts in the graft will survive (tis-
Wound healing and clinical outcomes in sue-genetic potential) and continue
suring technology for treatment out-
vascular beds
come evaluation allowed in to produce tissue-specific endoge-
particular to quantify the thickness If in contrast to soft tissue recession nous proteins (tissue-inductive prop-
of the marginal soft tissues estab- treatment SCTGs are used for soft erties) by receiving an adequate
lished above the formerly exposed tissue volume build-ups in terms of supply of oxygen and nutrients
root surfaces and in this way analyse ridge preservation procedures, soft quickly enough seem to be relatively
its influence on recession treatment tissue ridge augmentations or papilla good. This thinking model might at
outcomes. Twelve months after sur- re-constructions, the pre-requisites least in part allow to explain the suc-
gery, mean soft tissue thickness was for uneventful and fast wound heal- cessful application of SCTGs in plas-
1.69  0.63 mm and 0.910.18 mm, ing processes are comparatively tic periodontal and implant surgery
respectively, increased gingival thick- favourable as the blood supply for today. It might in addition be used
ness was clearly associated with bet- graft integration is provided by both to elucidate the aforementioned clini-
ter surgical outcomes in terms of the overlying flap and the recipient cal observation that SCTGs from
recession reduction and root cover- bed (Fig. 9). Although the terms os- different donor sites and harvested
age, whereas a mean marginal soft teoconduction, osteoinduction and with different techniques seem to
tissue thickness of 1.44 mm was nec- osteogenesis originate from concepts provide different properties regard-
essary to achieve complete root cov- of bone regeneration and bone heal- ing healing response and volume sta-
erage with a confidence of 95% ing, the underlying principles might bility. Furthermore, the clinical
(Rebele et al. submitted for publica- also be used to qualify the healing presumption can be supported that
tion). In a cohort of six SCTG and regeneration processes associ- among the available SCTGs those
patients within the same study popu- ated with soft tissue grafting. Equal appear to have a better wound heal-
lation healing dynamics were evalu- to bone grafts the ideal soft tissue ing response that seem to undergo
ated by means of volumetric graft should exhibit an optimal remarkable shrinkage, and vice
observations with the post-operative potential for tissue-specific conduc- versa. Considering its significance for
volume gain at 1 month being tion and induction as well and con- soft tissue augmentation procedures
regarded as baseline value. The trea- tain the largest number of co- in plastic periodontal and implant
ted sites showed a mean shrinkage transplanted vital cells possible. In surgery, it is remarkable that volu-
of 1/4 of the augmented volume after principle, SCTGs seem to have good metric aspects have been hardly eval-
3 months, amounting to 1/3 after characteristics with respect to the uated in the literature. Thus, to the
12 months corresponding to a mean above-mentioned requirements for best of our knowledge only two clin-
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Soft tissue replacement grafts S135

ical studies on volumetric changes Thalmair et al. 2013, Zuhr et al. role. Furthermore, it should be kept
after soft tissue ridge augmentation accepted for publication, Rebele in mind that the risk of graft necro-
procedures with a follow-up period et al. submitted for publication) sis might increase with graft thick-
of 3.5 months (Studer et al. 2000) offers new perspectives in this con- ness (Miller 1985, Borghetti &
and 12 months (Schneider et al. nection: If ongoing progress and Gardella 1990). Besides, those care
2011) presently exist. Studer and development regarding soft tissue should be taken that the blood clot
coworkers compared in a controlled augmentation procedures in plastic between wound bed and trans-
clinical study SCTGs and FGGs for periodontal and implant surgery is planted tissue is post-operatively as
soft tissue ridge augmentation by the goal, to volumetrically evaluate thin as possible to minimize diffu-
quantitative volume assessment. and compare the efficacy and long- sion distance and capillary prolifera-
Impressions were made before treat- term stability of eligible soft tissue tion length, and that the graft is
ment and also at 1 and 3.5 months replacement grafts will be one of the embedded stable and immobile in
after surgery to measure the volume main challenges for the future the recipient site by tension-free flaps
changes on dental casts with a vali- (Fig. 10). and appropriate suturing techniques
dated projection Moire system. Vol- The above-mentioned scientific (Allen & Miller 1989, Pini Prato
umetric assessment after 3.5 months investigations give a deep insight et al. 2000). In this context, a gentle
revealed significantly greater volume into the fundamental physiologic wound compression immediately fol-
gain with SCTGs in comparison to processes and the healing chronology lowing surgery might have a positive
FGGs (Studer et al. 2000). Schneider of free autogenous soft tissue grafts. effect and in-depth patient instruc-
and coworkers evaluated the dimen- In this respect, some factors of clini- tions on post-operative physical rest
sional changes of peri-implant tissues cal relevance can be identified that of the intra-oral wound area might
obtained by hard and soft tissue should be respected to accomplish also play a role.
augmentation. Impressions were successful and predictable treatment
taken before treatment, after implant outcomes if SCTGs are used in plas-
Soft tissue substitutes
placement and guided bone regener- tic periodontal and implant surgery.
ation, after soft tissue augmentation In the first place, the best possible Soft tissue augmentation procedures
with SCTGs, immediately after blood supply from the recipient bed with autogenous grafting materials
crown insertion and 1 year later. and the covering flap should be pro- have significant disadvantages. First
After the cast models were scanned vided for graft survival: incision- and foremost, the amount of avail-
and digitally superimposed, a and flap-design (Mormann & Cian- able tissue is limited and in the
mean buccal tissue gain of 1.27  cio 1977), thickness of the flap majority of clinical situations, a sec-
0.67 mm could be determined after (Hwang & Wang 2006), complete ond surgical site is needed to obtain
the surgical procedures. One year graft coverage (Harris 1994, Studer a sufficient quantity of autograft
after crown insertion, a mean loss of et al. 2000) and an atraumatic surgi- material, which increases the burden
0.04  0.31 mm in the labial direc- cal proceeding (Burkhardt & Lang on the patient and the morbidity of
tion was recorded. Guided bone 2005) seem to play an important the surgical procedure considerably
regeneration conducted more to vol- (Farnoush 1978, Del Pizzo et al.
ume gain than soft tissue grafting. 2002, Griffin et al. 2006, Soileau &
Moreover, in one-third of the Brannon 2006). Against this back-
implants, the soft tissue augmenta- ground, it is quite evident that the
tion did not contribute to the search for suitable soft tissue substi-
increased buccal volume at all tutes is currently at the centre of
(Schneider et al. 2011). Besides that enormous efforts by scientists and
long-term data on volumetric stabil- manufacturers, for the good of the
ity of soft tissue augmentations are patient.
missing completely. This might Yet, the development of adequate
partly be explained by the fact that soft tissue substitutes turns out to be
in the past only very complicated complicated: SCTGs are undoubt-
measurement technologies like the edly considered as the gold standard
optical projection Moire method for soft tissue volume augmentations
used by Studer and coworkers were in plastic periodontal and implant
available (Studer et al. 2000). How- surgery to date. However, the term
ever, the introduction of the afore- gold standard suggests a well-
mentioned recently developed new defined, consistent standard of har-
measuring methods employing three- vesting procedure. However, in fact
dimensional optical scanning and there seems to be no standardized
subsequent virtual superimposing protocol for SCTG removal from
procedures with a previously unfore- Fig. 10. For future research it will be
the palate. As elucidated above dif-
seen precision in the quantitative important to generate more three-dimen- ferent available donor sites and har-
evaluation of volumetric changes sional data after soft tissue augmentation vesting techniques result in
(Windisch et al. 2007, Fickl et al. procedures. Innovative methods using inconsistent types of SCTGs that
2008, Strebel et al. 2009, Thoma digital superimposing of models allow vary in their histological composi-
et al. 2010, Schneider et al. 2011, precise volumetric evaluation. tion potentially influencing their clin-
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
S136 Zuhr et al.

ical characteristics. Furthermore, it and was inferior to the combination 2004, Murata et al. 2008, Aroca
is difficult to develop alternatives to of coronally advanced flap and et al. 2009, Griffin & Cheung 2009).
SCTGs as long as their true impact SCTG (Cairo et al. 2008). Even Carney and coworkers investigated
on successful treatment outcomes is though, in addition, sufficient long- the combined effect of recombinant
not entirely clear. In some indica- term data are missing it needs to be human platelet-derived growth factor
tions the actual role of the graft is stated that the application of acellu- (rhPDGF) applied on ADM, with
obviously the volume increasing lar dermal substitutes seems to be the aim to promote faster re-vascu-
effect, for example. in soft tissue presently widespread and accepted larization of the ADM network
ridge augmentation procedures. In by many clinicians as an approved (Carney et al. 2012). After a 6-
other applications like, for example alternative to SCTGs in gingival month healing period, they found no
in soft tissue recession treatment in recession treatment (Gapski et al. statistically significant differences in
contrast the true nature of the 2005, Cairo et al. 2008, Moslemi the clinical outcomes, showing no
SCTG is as mentioned before et al. 2011, Schlee & Esposito 2011). benefit from adding PDGF to
not quite as clear. As long as the As on the other hand, only few ADM. McGuire and coworkers con-
SCTG is not clearly defined and as short-term observations from clinical ducted a RCT to compare coronally
long as important information case series exist, scientific evidence is advanced flap procedures for gingi-
regarding the true effect of the weak if ADM is supposed to be used val recession treatment through a
SCTG is lacking it will be very diffi- for soft tissue ridge augmentation growth factor-mediated approach
cult to develop substitutes that are procedures (Thoma et al. 2009). with either beta-tricalcium phosphate
supposed to measure up with the Care needs to be taken, moreover, if (b-TCP) + 0.3 mg/ml rhPDGF-BB
current gold standard. Not least on bigger dimensioned grafts are with a bioabsorbable collagen
these grounds it needs to be realized required: Folded or layered ADM wound healing dressing or SCTG.
that for the time being the develop- might impede vascularization and Moreover, recession defects were cre-
ment of SCTG substitute materials lead to extensive shrinkage (Batista ated in six teeth, each requiring
is still in its infancy. et al. 2001, Wei et al. 2002). Ethical extraction for orthodontic therapy,
In principal, three basic soft tis- concerns being an allograft from and treated with the same treatment
sue substitute materials of different human cadavers and the pretended modalities. Nine months after surgi-
origin can be distinguished: alloge- risk of disease transmission are cal correction, en bloc resections
neic (of human origin), xenogeneic remarkable counterpoints of the were obtained and examined
(from another species, e.g. of porcine material frequently subjected by histologically and by the use of
or bovine origin), and alloplastic (of patients. micro-CT. In the RCT, statistically
artificial origin) materials. At the Later on tissue-engineered cellu- significant results favouring the
moment a variety of available prod- lar dermal substitutes, including cel- SCTG were found regarding reces-
ucts are on the market, whereby it lular components and tissue-inducing sion depth reduction 6 months after
needs to be mentioned restrictively substances, came to the centre of sci- surgery. Histologic and microcom-
that only a few of them have proved entific attention. Wilson and puted tomography examination
scientifically documented success. coworkers investigated the safety revealed evidence of new cementum,
In the late 1980s acellular dermal and effectiveness of living human fi- PDL with inserting connective tissue
substitutes were introduced to the broblasts cultivated on polymer scaf- fibres and supporting alveolar bone
dental market. The best-researched folds compared with autogenous in all sites treated with rhPDGF-BB
type is the acellular dermal matrix SCTGs for gingival recession treat- + b-TCP, whereas neither SCTG-
(ADM), an allogeneic substitute that ment (Wilson et al. 2005). The treated site exhibited any signs of
consists of a freeze-dried connective 6-month results were promising with periodontal regeneration (McGuire
tissue matrix, without epithelium no statistically significant differences et al. 2009a).
and cellular components, which is between control and test group. Jha- Recently, xenogeneic soft tissue
obtained from tissue banks by a veri and coworkers, who applied substitutes in the shape of bilayered
standardized, controlled manufactur- autologous fibroblasts on ADM porcine-derived collagen-based
ing process. It contains type I- and scaffolds, found similar outcomes matrices were introduced. Although
III- collagen bundles and elastic compared with SCTGs in their these materials were originally intro-
fibres, which seem to be degraded investigation (Jhaveri et al. 2010). duced to promote keratinized tissue
and replaced by host tissues during Despite these promising findings, the regeneration (Sanz et al. 2009, Her-
the wound healing and integration critical cost-benefit ratio seems to ford et al. 2010, Nevins et al. 2011,
process (Wei et al. 2002, Cummings presently interfere with further Lorenzo et al. 2012), they were sub-
et al. 2005, Scarano et al. 2009). investments in this type of substitute sequently adopted for root coverage
With respect to root coverage proce- material. To what extent in the con- procedures. Clinical outcome mea-
dures, a systematic review by Cairo text of tissue-engineered soft tissue sures were promising in short-term
and coworkers revealed considerable substitutes growth factors in the view and a certain potential for soft
heterogeneity in clinical outcome form of platelet-rich fibrin mem- tissue thickening was observed,
measures after 612 months and branes or platelet-concentrated grafts although a lower percentage of root
concluded that adding ADM to cor- could be applied to replace SCTGs coverage was recorded compared
onally advanced pedicle flaps did not for gingival recession treatment is with coronally advanced flaps in
improve clinical results compared also a matter of current scientific combination with SCTGs (Cardaro-
with coronally advanced flaps alone investigations (Cheung & Griffin poli & Cardaropoli 2009, McGuire
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Soft tissue replacement grafts S137

& Scheyer 2010, Cardaropoli et al.


2012, Jepsen et al. 2013) (Fig. 11). A
surgery, future substitutes should in
addition feature tissue-genetic and
Up to date, the clinical decision
where to harvest SCTGs from is
new type of collagen matrix intended tissue-inductive properties. The hardly based on scientific evi-
to be used as a SCTG substitute for extent to which these properties dence but rather depends on the
large volume augmentations was might be improved, for example by amount of available tissue at the
recently investigated in an experi- adding autogenous cells and syn- eligible donor sites, the indication
mental study by Thoma and cowork- thetic growth proteins or bioactive in which the transplant is sup-
ers (Thoma et al. 2010). Soft tissue substances and the degree to which posed to be used and in particu-
ridge augmentation was performed innovative medical technologies such lar on the personal preference of
with either the substitute or SCTGs as tissue engineering might allow to the treating surgeon.
from the lateral palate. Impressions
were taken before augmentation and
use substitute materials more than to
date remain to be seen. The next
Independent of the selected
donor site the clinical procedure
at 28 and 84 days. In a forward- generation technology should aim of SCTG harvesting from the
looking way, the obtained casts were for soft tissue substitutes that are at palate is basically characterized
optically scanned and the digital least as good as or even better than by the challenge of obtaining an
images analysed. As volumetric SCTGs for soft tissue volume aug- adequate amount of tissue while
analysis demonstrated no statistically mentation by vascularizing quickly, minimizing postoperative pain
significant differences between both for instance by implementation of a and reducing the risk of compli-
groups the authors concluded that pre-fabricated vascular network cations at its best.
the experimental collagen matrix
might be a suitable device for soft
(Calcagni et al. 2011), by allowing
for healing by secondary intention,
The limited amount of grafting
tissue and the increased patient
tissue volume augmentation and and ideally by showing no post-oper- morbidity are substantial disad-
might serve as a substitute for autog- ative shrinkage at all. Like SCTGs vantages of autogenous SCTGs.
enous soft tissue to augment local- from different donor sites are at this For this reason, the search for
ized alveolar ridge defects. More stage utilized in various indications, suitable soft tissue substitutes is
clinical and in particular long-term it is conceivable that there is a need currently at the centre of numer-
studies will be needed to confirm to develop a variety of substitute ous efforts by scientists and man-
these promising results. materials with distinct properties ufacturers and will be an
Finally, eligible soft tissue substi- deployed in varying clinical situa- important field of future research
tutes must be non-infectious and tions at the end. for the good of the patient.
biocompatible. They should provide
good tissue integration behaviour
Many questions with regard to
Summary and conclusions graft healing and volumetric sta-
with tissue-conductive characteris- bility remain presently unknown
tics. Their mechanical properties The predominant interventions in this relates to soft tissue substi-
should assure good clinical handling plastic periodontal and implant sur- tutes, but to autologous SCTGs
and physical stability. They should gery are augmentation procedures as well. Patient-centred outcome
be economically efficient and docu- frequently performed by the use of measures, quantitative three-
mented success must be given. It will soft tissue replacement grafts. dimensional and qualitative-aes-
undoubtedly be of great importance Although written evidence lacks rele- thetic assessment of treatment
to develop soft tissue substitutes that vant data for the most part, the results as well as long-term fol-
can replace autogenous grafts in the present review demonstrates clearly low-up data are hardly available
near future. However, to completely that among available augmentation at present.
dispense with the need of autografts
for soft tissue volume augmentation
materials autologous SCTGs are
considered as the gold standard for
Thus, more research is needed to
further progress and increase
in plastic periodontal and implant soft tissue volume augmentation to knowledge regarding soft tissue
date. However, there is a restrictive volume augmentation procedures
core of critical elements that could in plastic periodontal and
be identified within the scope of this implant surgery. At the end, the
article and that can be summarized goal cannot be considerably dif-
as follows: ferent from developing appropri-
ate soft tissue substitutes for all
The term gold standard implies conceivable indications and by
a well-defined and consistent doing so rendering soft tissue
standard of harvesting procedure. autografts unnecessary and elimi-
Different donor sites at the palate nating their clinical application
that can be selected and varying to the best possible extent.
harvesting techniques that can be
applied, though, result in differ-
Fig. 11. Scanning electron microscope
image of a commercially available xeno- ent kinds of SCTGs that vary in
their histological composition References
geneic collagen matrix. The bilayered
design is supposed to provide tissue-con- obviously leading to different Abrahamsson, I., Berglundh, T., Glantz, P. O. &
ductive properties and good clinical han- characteristics that might require Lindhe, J. (1998) The mucosal attachment at
dling (courtesy of Peter Sch
upbach). selective clinical application. different abutments. An experimental study in

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
S138 Zuhr et al.

dogs. Journal of Clinical Periodontology 25, tional journal of periodontics & restorative results. Journal of Periodontology 75, 1678
721727. dentistry 14, 126137. 1687.
Agudio, G., Nieri, M., Rotundo, R., Franceschi, Bruno, J. F. & Bowers, G. M. (2000) Histology Cordioli, G., Mortarino, C., Chierico, A., Gruso-
D., Cortellini, P. & Pini Prato, G. P. (2009) of a human biopsy section following the place- vin, M. & Majzoub, Z. (2001) Comparison of 2
Periodontal conditions of sites treated with gin- ment of a subepithelial connective tissue graft. techniques of subepithelial connective tissue
gival-augmentation surgery compared to The International journal of periodontics & graft in the treatment of gingival recessions.
untreated contralateral homologous sites: a 10- restorative dentistry 20, 225231. Journal of Periodontology 72, 14701476.
to 27-year long-term study. Journal of Peri- Burkhardt, R., Joss, A. & Lang, N. P. (2008) Soft Corn, H. (1962) Periosteal separation - its clinical
odontology 80, 13991405. tissue dehiscence coverage around endosseous significance. Journal of Periodontology 33, 144
Allen, A. L. (1994) Use of the supraperiosteal implants: a prospective cohort study. Clinical 152.
envelope in soft tissue grafting for root cover- Oral Implants Research 19, 451457. Cortellini, P. & Pini Prato, G. (2012) Coronally
age. I. Rationale and technique. The Interna- Burkhardt, R. & Lang, N. P. (2005) Coverage of advanced flap and combination therapy for
tional journal of periodontics & restorative localized gingival recessions: comparison of root coverage. Clinical strategies based on sci-
dentistry 14, 216227. micro- and macrosurgical techniques. Journal entific evidence and clinical experience. Peri-
Allen, E. P. & Miller, P. D. Jr (1989) Coronal of Clinical Periodontology 32, 287293. odontology 2000 59, 158184.
positioning of existing gingiva: short term Cairo, F., Pagliaro, U. & Nieri, M. (2008) Cortellini, P., Tonetti, M., Baldi, C., Francetti,
results in the treatment of shallow marginal tis- Treatment of gingival recession with coronally L., Rasperini, G., Rotundo, R., Nieri, M.,
sue recession. Journal of Periodontology 60, advanced flap procedures: a systematic Franceschi, D., Labriola, A. & Prato, G. P.
316319. review. Journal of Clinical Periodontology 35, (2009) Does placement of a connective tissue
Al-Zahrani, M. S., Bissada, N. F., Ficara, A. J. & 136162. graft improve the outcomes of coronally
Cole, B. (2004) Effect of connective tissue graft Calcagni, M., Althaus, M. K., Knapik, A. D., advanced flap for coverage of single gingival
orientation on root coverage and gingival aug- Hegland, N., Contaldo, C., Giovanoli, P. & recessions in upper anterior teeth? A multi-cen-
mentation. The International journal of peri- Lindenblatt, N. (2011) In vivo visualization of tre, randomized, double-blind, clinical trial.
odontics & restorative dentistry 24, 6569. the origination of skin graft vasculature in a Journal of Clinical Periodontology 36, 6879.
Aroca, S., Keglevich, T., Barbieri, B., Gera, I. & wild-type/GFP crossover model. Microvascular Cummings, L. C., Kaldahl, W. B. & Allen, E. P.
Etienne, D. (2009) Clinical evaluation of a Research 82, 237245. (2005) Histologic evaluation of autogenous
modified coronally advanced flap alone or in Cardaropoli, D. & Cardaropoli, G. (2009) Heal- connective tissue and acellular dermal matrix
combination with a platelet-rich fibrin mem- ing of gingival recessions using a collagen grafts in humans. Journal of Periodontology 76,
brane for the treatment of adjacent multiple membrane with a hemineralized xenograft: a 178186.
gingival recessions: a 6-month study. Journal of randomized controlled clinical trial. The Inter- Del Pizzo, M., Modica, F., Bethaz, N., Priotto, P.
Periodontology 80, 244252. national journal of periodontics & restorative & Romagnoli, R. (2002) The connective tissue
Batista, E. L. Jr, Batista, F. C. & Novaes, A. B. dentistry 29, 5967. graft: a comparative clinical evaluation of
Jr (2001) Management of soft tissue ridge Cardaropoli, D., Tamagnone, L., Roffredo, A. & wound healing at the palatal donor site. A pre-
deformities with acellular dermal matrix. Clini- Gaveglio, L. (2012) Treatment of gingival liminary study. Journal of Clinical Periodontol-
cal approach and outcome after 6 months of recession defects using coronally advanced flap ogy 29, 848854.
treatment. Journal of Periodontology 72, with a porcine collagen matrix compared to Donn, B. J. Jr (1978) The free connective tissue
265273. coronally advanced flap with connective tissue autograft: a clinical and histologic wound heal-
Benninger, B., Andrews, K. & Carter, W. (2012) graft: a randomized controlled clinical trial. ing study in humans. Journal of Periodontology
Clinical measurements of hard palate and Journal of Periodontology 83, 321328. 49, 253260.
implications for subepithelial connective tissue Carney, C. M., Rossmann, J. A., Kerns, D. G., Dorfman, H. S., Kennedy, J. E. & Bird, W. C.
grafts with suggestions for palatal nomencla- Cipher, D. J., Rees, T. D., Solomon, E. S., Ri- (1982) Longitudinal evaluation of free autoge-
ture. Journal of Oral and Maxillofacial Surgery vera-Hidalgo, F. & Beach, M. M. (2012) A nous gingival grafts. A four year report. Jour-
70, 149153. comparative study of root defect coverage nal of Periodontology 53, 349352.
Berglundh, T., Lindhe, J., Ericsson, I., Marinello, using an acellular dermal matrix with and with- Edel, A. (1974) Clinical evaluation of free connec-
C. P., Liljenberg, B. & Thomsen, P. (1991) The out a recombinant human platelet-derived tive tissue grafts used to increase the width of
soft tissue barrier at implants and teeth. Clini- growth factor. Journal of Periodontology 83, keratinised gingiva. Journal of Clinical Peri-
cal Oral Implants Research 2, 8190. 893901. odontology 1, 185196.
Bernimoulin, J. P., Luscher, B. & Muhlemann, H. Carnio, J., Camargo, P. M. & Kenney, E. B. Eger, T., Muller, H. P. & Heinecke, A. (1996)
R. (1975) Coronally repositioned periodontal (2003) Root resorption associated with a sub- Ultrasonic determination of gingival thickness.
flap. Clinical evaluation after one year. Journal epithelial connective tissue graft for root cover- Subject variation and influence of tooth type
of Clinical Periodontology 2, 113. age: clinical and histologic report of a case. and clinical features. Journal of Clinical Peri-
Bohannan, H. M. (1962) Studies in the alteration The International journal of periodontics & odontology 23, 839845.
of vestibular depth. I. Complete denudation. restorative dentistry 23, 391398. Ericsson, I. & Lindhe, J. (1984) Recession in sites
Journal of Periodontology 33, 120128. Carnio, J., Camargo, P. M., Kenney, E. B. & with inadequate width of the keratinized gin-
Borghetti, A. & Gardella, J. P. (1990) Thick gingi- Schenk, R. K. (2002) Histological evaluation of giva. An experimental study in the dog. Journal
val autograft for the coverage of gingival reces- 4 cases of root coverage following a connective of Clinical Periodontology 11, 95103.
sion: a clinical evaluation. The International tissue graft combined with an enamel matrix Esposito, M., Maghaireh, H., Grusovin, M. G.,
journal of periodontics & restorative dentistry derivative preparation. Journal of Periodontol- Ziounas, I. & Worthington, H. V. (2012) Soft
10, 216229. ogy 73, 15341543. tissue management for dental implants: what
Borghetti, A. & Louise, F. (1994) Controlled clini- Carranza, F. A. Jr & Carraro, J. J. (1970) Muco- are the most effective techniques? A Cochrane
cal evaluation of the subpedicle connective tis- gingival techniques in periodontal surgery. systematic review. European Journal of Oral
sue graft for the coverage of gingival recession. Journal of Periodontology 41, 294299. Implantology 5, 221238.
Journal of Periodontology 65, 11071112. Chambrone, L., Pannuti, C. M., Tu, Y. K. & Farnoush, A. (1978) Techniques for the protec-
Bouchard, P., Etienne, D., Ouhayoun, J. P. & Chambrone, L. A. (2012) Evidence-based peri- tion and coverage of the donor sites in free soft
Nilveus, R. (1994) Subepithelial connective tis- odontal plastic surgery. II. An individual data tissue grafts. Journal of Periodontology 49, 403
sue grafts in the treatment of gingival reces- meta-analysis for evaluating factors in achiev- 405.
sions. A comparative study of 2 procedures. ing complete root coverage. Journal of Peri- Fickl, S., Zuhr, O., Wachtel, H., Bolz, W. & Hu-
Journal of Periodontology 65, 929936. odontology 83, 477490. erzeler, M. (2008) Tissue alterations after tooth
Bowers, G. M. (1963) A study of the width of Chambrone, L., Sukekava, F., Araujo, M. G., Pu- extraction with and without surgical trauma: a
attached gingiva. Journal of Periodontology 34, stiglioni, F. E., Chambrone, L. A. & Lima, L. volumetric study in the beagle dog. Journal of
201209. A. (2010) Root-coverage procedures for the Clinical Periodontology 35, 356363.
Bradley, R. E., Gant, J. C. & Ivancie, G. P. treatment of localized recession-type defects: a Friedman, N. (1962) Mucogingival surgery: The
(1959) Histologic evaluation of mucogingival Cochrane systematic review. Journal of Peri- apically repositioned flap. Journal of Periodon-
surgery. Oral Surgery, Oral Medicine, and Oral odontology 81, 452478. tology 33, 328340.
Pathology 12, 11841199. Cheung, W. S. & Griffin, T. J. (2004) A compara- Friedman, N. & Levine, H. L. (1964) Mucogingi-
Bruno, J. F. (1994) Connective tissue graft tech- tive study of root coverage with connective tis- val surgery. Current status. Journal of Peri-
nique assuring wide root coverage. The Interna- sue and platelet concentrate grafts: 8-month odontology 35, 521.

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Soft tissue replacement grafts S139

Fu, J. H., Hasso, D. G., Yeh, C. Y., Leong, D. the same location. The International journal of of soft tissues caused by restorative materials.
J., Chan, H. L. & Wang, H. L. (2011) The periodontics & restorative dentistry 27, 333339. The International journal of periodontics &
accuracy of identifying the greater palatine Herford, A. S., Akin, L., Cicciu, M., Maiorana, restorative dentistry 27, 251257.
neurovascular bundle: a cadaver study. Journal C. & Boyne, P. J. (2010) Use of a porcine col- Karring, T., Cumming, B. R., Oliver, R. C. &
of Periodontology 82, 10001006. lagen matrix as an alternative to autogenous Loe, H. (1975) The origin of granulation tissue
Gapski, R., Parks, C. A. & Wang, H. L. (2005) tissue for grafting oral soft tissue defects. and its impact on postoperative results of mu-
Acellular dermal matrix for mucogingival sur- Journal of Oral and Maxillofacial Surgery 68, cogingival surgery. Journal of Periodontology
gery: a meta-analysis. Journal of Periodontology 14631470. 46, 577585.
76, 18141822. Hokett, S. D., Peacock, M. E., Burns, W. T., Karring, T., Lang, N. R. & Loe, H. (1974) The
Gapski, R., Satheesh, K. & Cobb, C. M. (2006) Swiec, G. D. & Cuenin, M. F. (2002) External role of gingival connective tissue in determining
Histomorphometric analysis of bone density in root resorption following partial-thickness con- epithelial differentiation. Journal of Periodontal
the maxillary tuberosity of cadavers: a pilot nective tissue graft placement: a case report. Research 10, 111.
study. Journal of Periodontology 77, 10851090. Journal of Periodontology 73, 334339. Karring, T., Ostergaard, E. & Loe, H. (1971)
Gargiulo, A. W. & Arrocha, R. (1967) Histo-clini- Huang, L. H., Neiva, R. E., Soehren, S. E., Gian- Conservation of tissue specificity after hetero-
cal evaluation of free gingival grafts. Periodon- nobile, W. V. & Wang, H. L. (2005) The effect topic transplantation of gingiva and alveolar
tics 5, 285291. of platelet-rich plasma on the coronally mucosa. Journal of Periodontal Research 6,
Goldstein, M., Boyan, B. D., Cochran, D. L. & advanced flap root coverage procedure: a pilot 282293.
Schwartz, Z. (2001) Human histology of new human trial. Journal of Periodontology 76, Keceli, H. G., Sengun, D., Berberoglu, A. & Kar-
attachment after root coverage using subepithe- 17681777. abulut, E. (2008) Use of platelet gel with con-
lial connective tissue graft. Journal of Clinical Hurzeler, M. B. & Weng, D. (1999) A single-inci- nective tissue grafts for root coverage: a
Periodontology 28, 657662. sion technique to harvest subepithelial connec- randomized-controlled trial. Journal of Clinical
Gomes, S. C., Miranda, L. A., Soares, I. & Op- tive tissue grafts from the palate. The Periodontology 35, 255262.
permann, R. V. (2005) Clinical and histologic International journal of periodontics & restor- Kisch, J., Badersten, A. & Egelberg, J. (1986)
evaluation of the periodontal response to ative dentistry 19, 279287. Longitudinal observation of unattached,
restorative procedures in the dog. The Interna- Hwang, D. & Wang, H. L. (2006) Flap thickness mobile gingival areas. Journal of Clinical Peri-
tional journal of periodontics & restorative den- as a predictor of root coverage: a systematic odontology 13, 131134.
tistry 25, 3947. review. Journal of Periodontology 77, 1625 Klosek, S. K. & Rungruang, T. (2009) Anatomi-
Griffin, T. J. & Cheung, W. S. (2009) Guided tis- 1634. cal study of the greater palatine artery and
sue regeneration-based root coverage with a Ikuta, C. R., Cardoso, C. L., Ferreira-Junior, O., related structures of the palatal vault: consider-
platelet concentrate graft: a 3-year follow-up Lauris, J. R., Souza, P. H. & Rubira-Bullen, I. ations for palate as the subepithelial connective
case series. Journal of Periodontology 80, 1192 R. (2013) Position of the greater palatine fora- tissue graft donor site. Surgical and Radiologic
1199. men: an anatomical study through cone beam Anatomy 31, 245250.
Griffin, T. J., Cheung, W. S., Zavras, A. I. & computed tomography images. Surgical and Lafzi, A., Faramarzi, M., Shirmohammadi, A.,
Damoulis, P. D. (2006) Postoperative complica- Radiologic Anatomy 35, 837842. Behrozian, A., Kashefimehr, A. & Khashabi,
tions following gingival augmentation proce- Ivancie, G. P. (1957) Experimental and histologi- E. (2012) Subepithelial connective tissue graft
dures. Journal of Periodontology 77, 20702079. cal investigation of gingival regeneration in ves- with and without the use of plasma rich in
Guiha, R., el Khodeiry, S., Mota, L. & Caffesse, tibular surgery. Journal of Periodontology 28, growth factors for treating root exposure. Jour-
R. (2001) Histological evaluation of healing 259263. nal of Periodontal & Implant Science 42, 196
and revascularization of the subepithelial con- Jahnke, P. V., Sandifer, J. B., Gher, M. E., Gray, 203.
nective tissue graft. Journal of Periodontology J. L. & Richardson, A. C. (1993) Thick free Landsberg, C. J. & Bichacho, N. (1994) A modi-
72, 470478. gingival and connective tissue autografts for fied surgical/prosthetic approach for optimal
Haggerty, P. C. (1966) The use of a free gingival root coverage. Journal of Periodontology 64, single implant supported crown. Part IThe
graft to create a healthy environment for full 315322. socket seal surgery. Practical Periodontics and
crown preparation. Case history. Periodontics Jankovic, S., Aleksic, Z., Klokkevold, P., Lekovic, Aesthetic Dentistry 6, 1117; quiz 19.
4, 329331. V., Dimitrijevic, B., Kenney, E. B. & Camargo, Lang, N. P. & Loe, H. (1972) The relationship
Hall, W. B. (1981) The current status of mucogin- P. (2012) Use of platelet-rich fibrin membrane between the width of keratinized gingiva and
gival problems and their therapy. Journal of following treatment of gingival recession: a ran- gingival health. Journal of Periodontology 43,
Periodontology 52, 569575. domized clinical trial. The International journal 623627.
Hangorsky, U. & Bissada, N. F. (1980) Clinical of periodontics & restorative dentistry 32, e41 Lang, N. P., Pun, L., Lau, K. Y., Li, K. Y. &
assessment of free gingival graft effectiveness e50. Wong, M. C. (2012) A systematic review on
on the maintenance of periodontal health. Jansen, W. A., Ruben, M. P., Kramer, G. M., survival and success rates of implants placed
Journal of Periodontology 51, 274278. Bloom, A. A. & Turner, H. (1969) Develop- immediately into fresh extraction sockets after
Harris, R. J. (1992) The connective tissue and ment of the blood supply to split-thickness free at least 1 year. Clinical Oral Implants Research
partial thickness double pedicle graft: a predict- gingival autografts. Journal of Periodontology 23 (Suppl 5), 3966.
able method of obtaining root coverage. Jour- 39, 707716. Langer, B. & Calagna, L. (1980) The subepithelial
nal of Periodontology 63, 477486. Jepsen, K., Jepsen, S., Zucchelli, G., Stefanini, connective tissue graft. Journal of Prosthetic
Harris, R. J. (1994) The connective tissue with M., de Sanctis, M., Baldini, N., Greven, B., Dentistry 44, 363367.
partial thickness double pedicle graft: the Heinz, B., Wennstrom, J., Cassel, B., Vigno- Langer, B. & Calagna, L. J. (1982) The subepithe-
results of 100 consecutively-treated defects. letti, F. & Sanz, M. (2013) Treatment of gingi- lial connective tissue graft. A new approach to
Journal of Periodontology 65, 448461. val recession defects with a coronally advanced the enhancement of anterior cosmetics. The
Harris, R. J. (1997) A comparison of two flap and a xenogeneic collagen matrix: a multi- International journal of periodontics & restor-
techniques for obtaining a connective tissue center randomized clinical trial. Journal of Clin- ative dentistry 2, 2233.
graft from the palate. The International journal ical Periodontology 40, 8289. Langer, B. & Langer, L. (1985) Subepithelial con-
of periodontics & restorative dentistry 17, 260 Jhaveri, H. M., Chavan, M. S., Tomar, G. B., nective tissue graft technique for root coverage.
271. Deshmukh, V. L., Wani, M. R. & Miller, P. Journal of Periodontology 56, 715720.
Harris, R. J. (1999) Human histologic evaluation D. Jr (2010) Acellular dermal matrix seeded Lindenblatt, N., Calcagni, M., Contaldo, C.,
of root coverage obtained with a connective tis- with autologous gingival fibroblasts for the Menger, M. D., Giovanoli, P. & Vollmar, B.
sue with partial thickness double pedicle graft. treatment of gingival recession: a proof-of- (2008) A new model for studying the revascu-
A case report. Journal of Periodontology 70, concept study. Journal of Periodontology 81, larization of skin grafts in vivo: the role of
813821. 616625. angiogenesis. Plastic and Reconstructive Surgery
Harris, R. J. (2003) Histologic evaluation of con- Joly, J. C., Carvalho, A. M., da Silva, R. C., Cio- 122, 16691680.
nective tissue grafts in humans. The Interna- tti, D. L. & Cury, P. R. (2007) Root coverage Lindenblatt, N., Platz, U., Althaus, M., Hegland,
tional journal of periodontics & restorative in isolated gingival recessions using autograft N., Schmidt, C. A., Contaldo, C., Vollmar, B.,
dentistry 23, 575583. versus allograft: a pilot study. Journal of Peri- Giovanoli, P. & Calcagni, M. (2010) Tempo-
Harris, R. J., Harris, L. E., Harris, C. R. & Har- odontology 78, 10171022. rary angiogenic transformation of the skin
ris, A. J. (2007) Evaluation of root coverage Jung, R. E., Sailer, I., Hammerle, C. H., Attin, T. graft vasculature after reperfusion. Plastic and
with two connective tissue grafts obtained from & Schmidlin, P. (2007) In vitro color changes Reconstructive Surgery 126, 6170.

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
S140 Zuhr et al.

Lindhe, J. & Nyman, S. (1980) Alterations of the the maximum graft dimensions at the palatal Orban, B. J. (1957) Oral Histology and Embryol-
position of the marginal soft tissue following vault as a donor site. Journal of Periodontology ogy. St. Louis: C.V. Mosby Company.
periodontal surgery. Journal of Clinical Peri- 77, 899902. Orban, B. & Sicher, H. (1945) The oral mucosa.
odontology 7, 525530. Mormann, W., Bernimoulin, J. P. & Schmid, M. Journal of Dental Education 10, 94103.
Lorenzo, R., Garcia, V., Orsini, M., Martin, C. & O. (1975) Fluorescein angiography of free gin- Ouhayoun, J. P., Sawaf, M. H., Gofflaux, J. C.,
Sanz, M. (2012) Clinical efficacy of a xenoge- gival autografts. Journal of Clinical Periodontol- Etienne, D. & Forest, N. (1988) Re-epithelial-
neic collagen matrix in augmenting keratinized ogy 2, 177189. ization of a palatal connective tissue graft
mucosa around implants: a randomized Mormann, W. & Ciancio, S. G. (1977) Blood sup- transplanted in a non-keratinized alveolar
controlled prospective clinical trial. Clinical ply of human gingiva following periodontal mucosa: a histological and biochemical study
Oral Implants Research 23, 316324. surgery. A fluorescein angiographic study. in humans. Journal of Periodontal Research 23,
Lucchesi, J. A., Santos, V. R., Amaral, C. M., Pe- Journal of Periodontology 48, 681692. 127133.
ruzzo, D. C. & Duarte, P. M. (2007) Coronally Moslemi, N., Mousavi Jazi, M., Haghighati, F., Paolantonio, M., Dolci, M., Esposito, P., DAr-
positioned flap for treatment of restored root Morovati, S. P. & Jamali, R. (2011) Acellular chivio, D., Lisanti, L., Di Luccio, A. & Peri-
surfaces: a 6-month clinical evaluation. Journal dermal matrix allograft versus subepithelial netti, G. (2002) Subpedicle acellular dermal
of Periodontology 78, 615623. connective tissue graft in treatment of gingival matrix graft and autogenous connective tissue
Mackenzie, I. C. & Fusenig, N. E. (1983) Regener- recessions: a 5-year randomized clinical study. graft in the treatment of gingival recessions: a
ation of organized epithelial structure. The Jour- Journal of Clinical Periodontology 38, 1122 comparative 1-year clinical study. Journal of
nal of Investigative Dermatology 81, 189s194s. 1129. Periodontology 73, 12991307.
Majzoub, Z., Landi, L., Grusovin, M. G. & Muller, H. P., Schaller, N., Eger, T. & Heinecke, Pfeifer, J. S. (1963) The growth of gingival tissue
Cordioli, G. (2001) Histology of connective tis- A. (2000) Thickness of masticatory mucosa. over denuded bone. Journal of Periodontology
sue graft. A case report. Journal of Periodontol- Journal of Clinical Periodontology 27, 431436. 34, 1016.
ogy 72, 16071615. Murata, M., Okuda, K., Momose, M., Kubo, K., Pini Prato, G. P., Cairo, F., Nieri, M., France-
Martins, T., Bosco, A., Nobrega, F., Nagata, M., Kuroyanagi, Y. & Wolff, L. F. (2008) Root cov- schi, D., Rotundo, R. & Cortellini, P. (2010)
Garcia, V. & Fucini, S. (2007) Periodontal tis- erage with cultured gingival dermal substitute Coronally advanced flap versus connective tis-
sue response to coverage of root cavities composed of gingival fibroblasts and matrix: a sue graft in the treatment of multiple gingival
restored with resin materials: A histomorpho- case series. The International journal of periodon- recessions: a split-mouth study with a 5-year
metric study in dogs. Journal of Periodontology tics & restorative dentistry 28, 461467. follow-up. Journal of Clinical Periodontology
78, 10751082. Nabers, C. L. (1954) Repositioning the attached 37, 644650.
Matter, J. (1982) Free gingival grafts for the treat- gingiva. Journal of Periodontology 25, 3839. Pini Prato, G., Pagliaro, U., Baldi, C., Nieri, M.,
ment of gingival recession. A review of some Nabers, J. M. (1966) Free gingival grafts. Peri- Saletta, D., Cairo, F. & Cortellini, P. (2000)
techniques. Journal of Clinical Periodontology odontics 4, 243245. Coronally advanced flap procedure for root
9, 103114. Nelson, S. W. (1987) The subpedicle connective coverage. Flap with tension versus flap without
McGuire, M. K. & Cochran, D. L. (2003) Evalua- tissue graft. A bilaminar reconstructive proce- tension: a randomized controlled clinical study.
tion of human recession defects treated with dure for the coverage of denuded root surfaces. Journal of Periodontology 71, 188201.
coronally advanced flaps and either enamel Journal of Periodontology 58, 95102. Raetzke, P. B. (1985) Covering localized areas of
matrix derivative or connective tissue. Part 2: Nemcovsky, C. E. (2001) Interproximal papilla root exposure employing the envelope tech-
Histological evaluation. Journal of Periodontol- augmentation procedure: a novel surgical nique. Journal of Periodontology 56, 397402.
ogy 74, 11261135. approach and clinical evaluation of 10 consecu- Rasperini, G., Silvestri, M., Schenk, R. K. &
McGuire, M. K. & Scheyer, E. T. (2010) Xenoge- tive procedures. The International journal of Nevins, M. L. (2000) Clinical and histologic
neic collagen matrix with coronally advanced periodontics & restorative dentistry 21, 553559. evaluation of human gingival recession treated
flap compared to connective tissue with coro- Nevins, M., Nevins, M. L., Kim, S. W., Schup- with a subepithelial connective tissue graft and
nally advanced flap for the treatment of dehis- bach, P. & Kim, D. M. (2011) The use of mu- enamel matrix derivative (Emdogain): a case
cence-type recession defects. Journal of cograft collagen matrix to augment the zone of report. The International journal of periodontics
Periodontology 81, 11081117. keratinized tissue around teeth: a pilot study. & restorative dentistry 20, 269275.
McGuire, M. K., Scheyer, E. T. & Schupbach, P. The International journal of periodontics & Reiser, G. M., Bruno, J. F., Mahan, P. E. & Lar-
(2009a) Growth factor-mediated treatment of restorative dentistry 31, 367373. kin, L. H. (1996) The subepithelial connective
recession defects: a randomized controlled trial Nickles, K., Ratka-Kruger, P., Neukranz, E., tissue graft palatal donor site: anatomic consid-
and histologic and microcomputed tomography Raetzke, P. & Eickholz, P. (2010) Ten-year erations for surgeons. The International journal
examination. Journal of Periodontology 80, results after connective tissue grafts and guided of periodontics & restorative dentistry 16, 130
550564. tissue regeneration for root coverage. Journal 137.
McGuire, M. K., Scheyer, T., Nevins, M. & of Periodontology 81, 827836. Roccuzzo, M., Bunino, M., Needleman, I. &
Schupbach, P. (2009b) Evaluation of human Nobuto, T. (1986) Microvascularization of the Sanz, M. (2002) Periodontal plastic surgery for
recession defects treated with coronally free gingival autograft using corrosion casts. treatment of localized gingival recessions: a sys-
advanced flaps and either purified recombinant Journal of Dental Research 65, 528. tematic review. Journal of Clinical Periodontol-
human platelet-derived growth factor-BB with Nobuto, T. (1987) Experimental study on micro- ogy 29 Suppl 3, 178194; discussion 195176.
beta tricalcium phosphate or connective tissue: vascularization following free gingival auto- Roccuzzo, M., Gaudioso, L., Bunino, M. &
a histologic and microcomputed tomographic graftprocess of the recirculation to grafts. Dalmasso, P. (2013) Surgical treatment of buc-
examination. The International journal of peri- Nihon Shishubyo Gakkai Kaishi 29, 352364. cal soft tissue recessions around single
odontics & restorative dentistry 29, 721. Nobuto, T., Imai, H. & Yamaoka, A. (1988) Mi- implants: 1-year results from a prospective pilot
Miller, P. D. Jr (1982) Root coverage using a free crovascularization of the free gingival auto- study. Clinical Oral Implants Research doi: 10.
soft tissue autograft following citric acid applica- graft. Journal of Periodontology 59, 639646. 1111/clr.12149. [Epub ahead of print].
tion. Part 1: Technique. The International journal Nordland, W. P., Sandhu, H. S. & Perio, C. Salkin, L. M., Freedman, A. L., Stein, M. D. &
of periodontics & restorative dentistry 2, 6570. (2008) Microsurgical technique for augmenta- Bassiouny, M. A. (1987) A longitudinal study
Miller, P. D. Jr (1985) Root coverage using the tion of the interdental papilla: three case of untreated mucogingival defects. Journal of
free soft tissue autograft following citric acid reports. The International journal of periodontics Periodontology 58, 164166.
application. III. A successful and predictable & restorative dentistry 28, 543549. Santamaria, M. P., Ambrosano, G. M., Casati,
procedure in areas of deep-wide recession. The Oates, T. W., Robinson, M. & Gunsolley, J. C. M. Z., Nociti Junior, F. H., Sallum, A. W. &
International journal of periodontics & restor- (2003) Surgical therapies for the treatment of Sallum, E. A. (2009) Connective tissue graft
ative dentistry 5, 1437. gingival recession. A systematic review. Annals plus resin-modified glass ionomer restoration
Miyasato, M., Crigger, M. & Egelberg, J. (1977) of Periodontology 8, 303320. for the treatment of gingival recession associ-
Gingival condition in areas of minimal and Ochsenbein, C. (1960) Newer concept of mucogin- ated with non-carious cervical lesion: a ran-
appreciable width of keratinized gingiva. Jour- gival surgery. Journal of Periodontology 31, domized-controlled clinical trial. Journal of
nal of Clinical Periodontology 4, 200209. 175185. Clinical Periodontology 36, 791798.
Monnet-Corti, V., Santini, A., Glise, J. M., Fou- Oliver, R. C., Loe, H. & Karring, T. (1968) Santamaria, M. P., Suaid, F. F., Casati, M. Z.,
que-Deruelle, C., Dillier, F. L., Liebart, M. F. Microscopic evaluation of the healing and Nociti, F. H., Sallum, A. W. & Sallum, E. A.
& Borghetti, A. (2006) Connective tissue graft revascularization of free gingival grafts. Journal (2008) Coronally positioned flap plus resin-
for gingival recession treatment: assessment of of Periodontal Research 3, 8495. modified glass ionomer restoration for the

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Soft tissue replacement grafts S141

treatment of gingival recession associated with flap surgery in dogs. Journal of Periodontology tions to orthodontic tooth movement in
non-carious cervical lesions: a randomized con- 33, 5669. monkeys. Journal of Clinical Periodontology 14,
trolled clinical trial. Journal of Periodontology Steiner, G. G., Pearson, J. K. & Ainamo, J. 121129.
79, 621628. (1981) Changes of the marginal periodontium Wessel, J. R. & Tatakis, D. N. (2008) Patient out-
Sanz, I., Garcia-Gargallo, M., Herrera, D., Mar- as a result of labial tooth movement in comes following subepithelial connective tissue
tin, C., Figuero, E. & Sanz, M. (2012) Surgical monkeys. Journal of Periodontology 52, 314 graft and free gingival graft procedures. Journal
protocols for early implant placement in post- 320. of Periodontology 79, 425430.
extraction sockets: a systematic review. Clinical Strebel, J., Ender, A., Paque, F., Krahenmann, Wilderman, M. N. (1964) Exposure of bone in
Oral Implants Research 23 (Suppl 5), 6779. M., Attin, T. & Schmidlin, P. R. (2009) In vivo periodontal surgery. Dental Clinics of North
Sanz, M., Lorenzo, R., Aranda, J. J., Martin, C. validation of a three-dimensional optical America 8, 2331.
& Orsini, M. (2009) Clinical evaluation of a method to document volumetric soft tissue Wilson, T. G. Jr, McGuire, M. K. & Nunn, M.
new collagen matrix (Mucograft prototype) to changes of the interdental papilla. Journal of E. (2005) Evaluation of the safety and efficacy
enhance the width of keratinized tissue in Periodontology 80, 5661. of periodontal applications of a living tissue-
patients with fixed prosthetic restorations: a Studer, S. P., Allen, E. P., Rees, T. C. & Kouba, engineered human fibroblast-derived dermal
randomized prospective clinical trial. Journal of A. (1997) The thickness of masticatory mucosa substitute. II. Comparison to the subepithelial
Clinical Periodontology 36, 868876. in the human hard palate and tuberosity as connective tissue graft: a randomized controlled
Scarano, A., Barros, R. R., Iezzi, G., Piattelli, A. potential donor sites for ridge augmentation feasibility study. Journal of Periodontology 76,
& Novaes, A. B. Jr (2009) Acellular dermal procedures. Journal of Periodontology 68, 145 881889.
matrix graft for gingival augmentation: a preli- 151. Windisch, S. I., Jung, R. E., Sailer, I., Studer, S.
minary clinical, histologic, and ultrastructural Studer, S. P., Lehner, C., Bucher, A. & Scharer, P., Ender, A. & Hammerle, C. H. (2007) A
evaluation. Journal of Periodontology 80, 253 P. (2000) Soft tissue correction of a single- new optical method to evaluate three-dimen-
259. tooth pontic space: a comparative quantitative sional volume changes of alveolar contours: a
Schatzle, M., Land, N. P., Anerud, A., Boysen, volume assessment. Journal of Prosthetic Den- methodological in vitro study. Clinical Oral
H., Burgin, W. & Loe, H. (2001) The influence tistry 83, 402411. Implants Research 18, 545551.
of margins of restorations of the periodontal Sullivan, H. C. & Atkins, J. H. (1968) Free autog- Yotnuengnit, P., Promsudthi, A., Teparat, T., Lao-
tissues over 26 years. Journal of Clinical Peri- enous gingival grafts. III. Ultilzation of grafts hapand, P. & Yuwaprecha, W. (2004) Relative
odontology 28, 5764. in the treatment of gingival recession. Periodon- connective tissue graft size affects root coverage
Schlee, M. & Esposito, M. (2011) Human dermis tics 6, 152160. treatment outcome in the envelope procedure.
graft versus autogenous connective tissue grafts Sullivan, H. C. & Atkins, J. H. (1969) The role of Journal of Periodontology 75, 886892.
for thickening soft tissue and covering multiple free gingival grafts in periodontal therapy. Den- Zucchelli, G. (2013) Mucogingival Esthetic Sur-
gingival recessions: 6-month results from a tal Clinics of North America 13, 133148. gery. Milan: Quintessenza Ediziono S.r.l.
preference clinical trial. European Journal of Thalmair, T., Fickl, S., Schneider, D., Hinze, Zucchelli, G., Amore, C., Sforza, N. M., Monte-
Oral Implantology 4, 119125. M. & Wachtel, H. (2013) Dimensional altera- bugnoli, L. & De Sanctis, M. (2003) Bilaminar
Schneider, D., Grunder, U., Ender, A., Hammer- tions of extraction sites after different alveolar techniques for the treatment of recession-type
le, C. H. & Jung, R. E. (2011) Volume gain ridge preservation techniques - a volumetric defects. A comparative clinical study. Journal
and stability of peri-implant tissue following study. Journal of Clinical Periodontology 40, of Clinical Periodontology 30, 862870.
bone and soft tissue augmentation: 1-year 721727. Zucchelli, G., Mazzotti, C., Mounssif, I., Mele,
results from a prospective cohort study. Clini- Thoma, D. S., Benic, G. I., Zwahlen, M., Ham- M., Stefanini, M. & Montebugnoli, L. (2013)
cal Oral Implants Research 22, 2837. merle, C. H. & Jung, R. E. (2009) A systematic A novel surgical-prosthetic approach for soft
Schoo, W. H. & van der Velden, U. (1985) Mar- review assessing soft tissue augmentation tech- tissue dehiscence coverage around single
ginal soft tissue recessions with and without niques. Clinical Oral Implants Research 20 implant. Clinical Oral Implants Research 24,
attached gingiva. A five year longitudinal (Suppl 4), 146165. 957962.
study. Journal of Periodontal Research 20, 209 Thoma, D. S., Jung, R. E., Schneider, D., Coch- Zucchelli, G., Mele, M., Stefanini, M., Mazzotti,
211. ran, D. L., Ender, A., Jones, A. A., Gorlach, C., Marzadori, M., Montebugnoli, L. & de
Seibert, J. S. (1983) Reconstruction of deformed, C., Uebersax, L., Graf-Hausner, U. & Ham- Sanctis, M. (2010) Patient morbidity and root
partially edentulous ridges, using full thickness merle, C. H. (2010) Soft tissue volume augmen- coverage outcome after subepithelial connective
onlay grafts. Part II. Prosthetic/periodontal tation by the use of collagen-based matrices: a tissue and de-epithelialized grafts: a compara-
interrelationships. Compendium of Continuing volumetric analysis. Journal of Clinical Peri- tive randomized-controlled clinical trial. Jour-
Education in Dentistry 4, 549562. odontology 37, 659666. nal of Clinical Periodontology 37, 728738.
Sharma, N. A. & Garud, R. S. (2013) Greater Thoma, D. S., Sancho-Puchades, M., Ettlin, D. Zuhr, O. & H urzeler, M. (2012) Plastic-Esthetic
palatine foramenkey to successful hemimaxil- A., Hammerle, C. H. & Jung, R. E. (2012) Periodontal and Implant Surgery - A Microsur-
lary anaesthesia: a morphometric study and Impact of a collagen matrix on early healing, gical Approach. Ltd: Quintessence Publishing
report of a rare aberration. Singapore Medical aesthetics and patient morbidity in oral muco- Co.
Journal 54, 152159. sal wounds - a randomized study in humans. Zuhr, O., Rebele, S., Schneider, D., Jung, R. &
da Silva, R. C., Joly, J. C., de Lima, A. F. & Ta- Journal of Clinical Periodontology 39, 157165. H urzeler, M. (2013) Tunnel technique with
takis, D. N. (2004) Root coverage using the de Trey, E. & Bernimoulin, J. P. (1980) Influence connective tissue graft versus coronally
coronally positioned flap with or without a of free gingival grafts on the health of the mar- advanced flap with enamel matrix derivate for
subepithelial connective tissue graft. Journal of ginal gingiva. Journal of Clinical Periodontology root coverage: a RCT using 3D digital measur-
Periodontology 75, 413419. 7, 381393. ing methods. Part I. Clinical and patient-cen-
Soileau, K. M. & Brannon, R. B. (2006) A histo- Wei, P. C., Laurell, L., Lingen, M. W. & Geivelis, tered outcomes. Journal of Clinical
logic evaluation of various stages of palatal M. (2002) Acellular dermal matrix allografts to Periodontology doi: 10.1111/jcpe.12178. [Epub
healing following subepithelial connective tis- achieve increased attached gingiva. Part 2. A ahead of print].
sue grafting procedures: a comparison of eight histological comparative study. Journal of Peri-
cases. Journal of Periodontology 77, 1267 odontology 73, 257265.
1273. Weng, D., H urzeler, M., Quinones, C., Pechstadt, Address:
Song, J. E., Um, Y. J., Kim, C. S., Choi, S. H., B., Mota, L. & Caffesse, R. (1998) Healing pat- Otto Zuhr
Cho, K. S., Kim, C. K., Chai, J. K. & Jung, terns in recession defects treated with ePTFE Private Practive H
urzeler/Zuhr
U. W. (2008) Thickness of posterior palatal membranes and with free connective tissue
masticatory mucosa: the use of computerized grafts. A histologic and histometric study in
Rosenkavalierplatz 18
tomography. Journal of Periodontology 79, the beagle dog. Journal of Clinical Periodontol- 81925 Munich
406412. ogy 25, 238245. Germany
Staffileno, H., Wentz, F. M. & Orban, B. (1962) Wennstrom, J. L., Lindhe, J., Sinclair, F. & Thi- E-Mail: o.zuhr@huerzelerzuhr.com
Histologic study of healing of split thickness lander, B. (1987) Some periodontal tissue reac-

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
S142 Zuhr et al.

Clinical relevance concerning the use of soft tissue Practical implications: The avail-
Scientific rationale: Soft tissue aug- replacement grafts. able donor sites provide grafts of
mentation procedures are increas- Principal findings: Subepithelial con- distinct shape and composition.
ingly performed in plastic nective tissue grafts are considered Which donor site is chosen depends
periodontal and implant surgery. as gold standard. Many questions on the amount of required tissue
Standardized guidelines regarding regarding graft healing and volumet- and the indication. Harvesting and
donor sites and harvesting tech- ric stability are presently unknown. transplantation procedures should
niques can hardly be given to date, The limited amount of grafting tis- follow certain advices to allow the
but recommendations for predict- sue and the increased patient mor- best healing and tissue integration
able treatment outcomes can be bidity make the search for suitable possible.
developed. The aim was to provide soft tissue substitutes an important
a narrative review of the literature field of future research.

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

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