e245

Epithelial Inclusions Following a Bilaminar Root Coverage

Procedure with a Subepithelial Connective Tissue Graft:
A Histologic and Clinical Study

Federica Romano, DDS1 Gingival recession is a frequent oc-

Stefano Perotto, DDS2 currence in patients with a high stan-
Luca Cricenti, DDS3 dard of oral hygiene, affecting single
Stefano Gotti, PhD4 or multiple root surfaces at all tooth
Mario Aimetti, MD, DDS5 types.1,2 Root hypersensitivity, es-
thetic problems, and abrasion may
The aim of this study was to histologically examine any epithelial cell inclusions accompany gingival recessions and
in submerged subepithelial connective tissue graft (SCTG) after clinical healing lead patients to seek treatment. The
was achieved. A total of 16 patients with Miller Class I or II gingival recessions ultimate goal of root coverage pro-
were consecutively treated with a bilaminar procedure. At 2 months after
cedures is complete and predictable
surgery, a gingival tissue specimen was harvested from all SCTG-treated
sites and stained with hematoxylin-eosin. The histologic evaluation revealed coronal displacement of the gingival
connective tissue in active reorganization without epithelial inclusions in 14 margin on the root surface. Recent
of the 16 tissue specimens. In the remaining 2 specimens, epithelial islands systematic reviews reported the best
were observed deep in the connective tissue. In one case they developed in predictability in complete root cover-
a solid cystic space, while in the second case they were strictly integrated in age when single or adjacent Miller
the lamina propria. Complete recession coverage was obtained in 14 of the
Class I and II recession defects were
16 treated defects, with a mean root coverage of 95.1% ± 14.2% at 12 months.
Int J Periodontics Restorative Dent 2017;37:e245–e252. doi: 10.11607/prd.3189 treated by subepithelial connective
tissue graft (SCTG) combined with
coronally advanced flap (CAF).3,4 A
large number of trials demonstrated
clinical safety and tolerability for pa-
tients of this procedure,5–7 whereas
only a few studies focused on the his-
tologic wound healing process. Most
of them are case reports in human8,9
or animal studies10,11 that analyzed
either the pattern of revasculariza-
Academic Researcher, Department of Surgical Sciences, CIR Dental School,
1
tion or the nature of the interface be-
Section of Periodontology, University of Turin, Turin, Italy.
2Private Practice, Turin, Italy.
tween the graft and the root surface.
3Clinical Instructor, Department of Surgical Sciences, CIR Dental School, A limited number of case reports
Section of Periodontology, University of Turin, Turin, Italy. described clinically and histologi-
4Academic Researcher, Department of Neurosciences, University of Turin, Turin, Italy.
cally incidental complications of the
5Associate Professor, Department of Surgical Sciences, CIR Dental School,

Section of Periodontology, University of Turin, Turin, Italy.

epithelial origin of SCTG. These in-
cluded root resorption,12 exostosis,13
Correspondence to: Prof Mario Aimetti, Section of Periodontology, CIR Dental School, and cyst or cystlike formation14–16
Via Nizza, 230, Turin 10126, Italy. Fax: +390116331506.
that occurred between 4 months
Email: mario.aimetti@unito.it
and 5 years postoperatively. These
©2017 by Quintessence Publishing Co Inc. complications were documented

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e246
only when the lesions were symp-
tomatic or associated with morpho-
logic tissue alterations.
Based on the findings of Harris,17
who identified epithelial remnants in
80% of the palatal connective tis-
sue grafts (CTGs) at the time of tis-
sue harvesting, a higher occurrence
of morphostructural alterations in
the healed donor tissue than that
reported in the literature could be
hypothesized. Therefore, the aim of
the present study was to histologi-
cally analyze any epithelial remnants
present in the grafted tissue in pa-
tients treated by submerged SCTG
for root coverage after clinical heal-
ing was achieved.
Materials and Methods
Patients and Root Coverage
Procedure
A total of 16 patients (5 men and 11
women; mean age 34.1 ± 6.9 years)
with esthetic and/or hypersensitiv-
ity complaints due to Miller Class I
and II recession defects participat-
ing in a prospective study on rein-
nervation and revascularization after
a SCTG root coverage procedure18
were histologically analyzed for mor-
phostructural alterations. They were
consecutively selected from among
individuals referred to the Section of
Periodontology, CIR Dental School,
Department of Surgical Sciences,
University of Turin, Italy, for root cov-
erage of localized gingival recessions
in the maxillary anterior region. Pa-
tients with systemic diseases contra-
indicating the periodontal surgery,
smokers, and pregnant and lactat-
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ing women were excluded from the
study. The study was conducted ac-
cording to the guidelines of the Dec-
laration of Helsinki and approved by
the Institutional Ethics Committee
(Protocol no. 00001521). Participants
received detailed information and
signed informed consent.
Data on the study design were
reported in the previous study.18
All patients received instruction in
proper nontraumatic tooth brushing
technique and supra- and subgin-
gival scaling with ultrasonic instru-
ments. The exposed root surfaces
were polished at low speed with
a rubber cup and a low-abrasive
polishing paste. Surgical treatment
of the recession defects was not
scheduled until the patient could
demonstrate a full-mouth plaque
score (FMPS) and a full-mouth
bleeding score (FMBS) ≤ 20%.
The same experienced clinician
(L.C.) performed all surgeries with
the aid of an operating microscope
(Zeiss S7). All gingival recessions were
treated by means of CAF in combina-
tion with SCTG resulting from the ex-
traoral de-epithelialization with a 15C
blade (under ×4 magnification) of a
free gingival graft (FGG).7,19 The FGG
was harvested from the palate using
the two parallel incisions approach in
the area between the distal aspect
of the canine and the distal aspect
of the first molar.20,21 The graft was
positioned at the cementoenamel
junction (CEJ), and the flap was coro-
nally displaced 2 mm above the CEJ.
Patients were instructed not to brush
their teeth in the treated area for 2
weeks but to rinse with chlorhexi-
dine digluconate 0.12% for 1 minute
twice daily. Sutures were removed at
2 weeks. After this period, patients
were instructed to use a soft tooth-
brush with a roll technique and were
placed on maintenance therapy for
the first postoperative year.
Tissue Collection and
Histologic Analysis
At 2 months after the root coverage
procedure, during a gingivoplasty
to improve soft tissue appearance,
an epithelium–connective tissue
(2 × 2 mm) specimen was collect-
ed from all SCTG-treated sites with
a microsurgical blade (USM 6700,
Sable Industries). An incision was
made at least 2 to 3 mm away from
the gingival margin in the attached
gingiva (Fig 1). Upon excision, the
biopsy area was protected with fi-
brillar collagen (Avitene, Bard Davol)
and tissue specimens were quickly
immersed in fixative (4% parafor-
maldehyde in 0.1-M phosphate buf-
fer [PBS], pH 7.35) and stored for
24 hours at 4°C. They were then
washed in 0.01-M PBS and placed
overnight at 4°C and finally in a 30%
sucrose solution in PBS for 3 days at
4°C. The specimens were frozen for
cryostat sectioning. Specimens were
serially cut at 25-µm thickness with a
Leica CM1900 cryostat and stained
with hematoxylin-eosin (h&e) using
standard procedure. Sections were
dried, cleared in xylene, and cover
slipped with Entellan (Merck). They
were examined and photographed
at ×10 and ×20 magnification using
a Nikon Eclipse 80i microscope con-
nected to a Nikon DS-Fi digital video
camera. All images were processed
using Adobe Photoshop CS4.
 e247

Fig 1 (a) Tissue specimen harvested for histologic analysis. (b) Dimensions of the tissue
specimen. (c) Healing after 6 months.

a b c

Fig 2 Histologic section (h&e) of a tissue

specimen after 2 months of healing. (a)
Keratinized epithelial tissue with elongated
rete pegs (×20 magnification). (b) Evidence
of active collagen deposition and newly
formed large vessels without epithelial
remnants (×10 magnification).

a b

Clinical Measurements
The following clinical parameters
were assessed at baseline and at
the 12-month follow-up visit using a
manual 1-mm graduated periodon-
tal probe (PCP-UNC 15, Hu-Friedy)
at the teeth included in the study: (1)
presence/absence of plaque (Plaque
Index [PI]), (2) presence/absence of
bleeding on probing (BoP), (3) re-
cession depth (RD) measured from
the CEJ to the most apical exten-
sion of the gingival margin at the
midbuccal aspect of the experimen-
tal tooth, (4) recession width (RW)
measured at the level of the CEJ,
(5) probing depth (PD) measured at
the midbuccal aspect of the study
tooth from the gingival margin to
the bottom of the sulcus, (6) clinical
attachment level (CAL) measured at
the midbuccal aspect of the study
tooth from the CEJ to the bottom of
the sulcus, and (7) keratinized tissue
(KT) measured from the most apical
point of the gingival margin to the
mucogingival junction. FMPS and
FMBS were also recorded.
Statistical Analysis
Clinical data were expressed as
mean ± SD. Due to the normal dis-
tribution of the parameters, Student
paired t test was used to compare
baseline and 12-month postsurgery
measurements. P < .05 was con-
sidered statistically significant. A
computer program was used for all
statistical analysis (SAS version 9.0,
SAS Institute).
Results
Healing was uneventful. At 2
months after surgery, gingival tis-
sue appeared clinically normal on
all experimental teeth, apart from
the unsatisfactory soft tissue tex-
ture that required gingivoplasty.
Histologically, all SCTG-treated

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e248

Fig 3 Histologic section (h&e) of a tissue specimen after 2 months of healing. (left) A solid cystic cavity (c) in the connective tissue. The cyst
wall was formed by stratified squamous epithelium (e) and surrounded by a thin layer of fibrous tissue. Below the cyst, some blood vessels
are visible (white arrows) (×4 magnification). (right) High magnification of image on left (×10 magnification).

case, the epithelial cell inclusion

Table 1 Clinical Parameters at Baseline and 12 Months Postsurgery
was strictly integrated in the sur-
Parameter Baseline 12 mo Difference P* rounding connective tissue. It had
FMPS (%) 15.2 ± 2.7 14.7 ± 2.5 0.5 ± 3.2 .634 a typical aspect of stratified squa-
FMBS (%) 12.8 ± 3.3 12.0 ± 3.6 0.8 ± 4.7 .616 mous epithelium and a well vascu-
RD (mm) 3.5 ± 1.3 0.2 ± 0.6 3.3 ± 1.4 < .001 larized surface with several blood
RW (mm) 3.5 ± 1.2 0.4 ± 1.1 3.1 ± 1.5 < .001 vessels running in the deep part of
the connective layer and in the con-
PD (mm) 1.2 ± 0.7 1.1 ± 0.5 0.1 ± 0.8 .751
nective papillae. The boundary be-
CAL (mm) 4.7 ± 1.5 1.4 ± 0.9 3.3 ±1.5 < .001
tween epithelium and connective
KT (mm) 2.9 ± 1.0 5.7 ± 1.3 -2.8 ± 1.1 < .001
layer had a wavy course with deep
FMPS = full-mouth plaque score; FMBS = full-mouth bleeding score;
RD = recession depth; RW = recession width; PD = probing depth; epithelial projections separated by
CAL = clinical attachment level; KT = height of keratinized tissue. connective papillae (Fig 4). On the
*Student paired t test.
outer side, granulation tissue with a
marked inflammatory infiltrate sur-
rounded the epithelial surface.
sites were characterized by con- (Fig 2b). Epithelial inclusions were Clinical data are reported in
nective tissue covered with kera- detected in the deep portion of Table 1. There was a significant re-
tinized epithelium with elongated the connective tissue in 2 out of 16 duction from baseline to 12-month
rete pegs (Fig 2a). H&e analysis tissue samples examined (12.5%). follow-up in RD, RW, and CAL
revealed the presence of collagen In one specimen, they developed (P < .001) in all treated defects. The
deposition with evidence of newly in a solid cystic cavity that was in- gingival appearance was satisfac-
formed large vessels in the most ternally lined by epithelial cells tory at 12 months. Complete root
apical portion of the connective tis- whose morphology was suggestive coverage was obtained in 14 out of
sue. A sharp demarcation line was of squamous stratified epithelium 16 recession defects, with a mean
still detectable between the graft- and externally by a thin layer of fi- percent root coverage of 95.1% ±
ed tissue and the recipient site flap brous tissue (Fig 3). In the second 14.2% (Fig 5).

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 e249

Fig 4 Histologic section (h&e) of a tissue specimen after 2 months of healing. (left) An inclusion of stratified squamous epithelium (e)
strictly integrated in the connective tissue (×4 magnification). On the outer side was a granulation tissue (g) with a marked inflammatory
infiltrate separating epithelial cells from the overlying connective tissue, whereas on the inner side some papillae interdigitations (p)
between epithelium and connective tissue were evident. White arrows = blood vessels. (right) High magnification of image on left (×10
magnification).

Fig 5 (left) Baseline gingival recession on a maxillary canine (histologic image in Fig 2). (right) View at 12 months postoperative, showing
complete root coverage, increased keratinized tissue, and a satisfactory esthetic outcome.

Discussion
The present study documents a
12.5% occurrence of epithelial cell
inclusions at the recipient site fol-
lowing a bilaminar procedure. After
a healing period of 2 months, 2 of
the 16 treated recession defects
presented histologic anomalies of
epithelial origin in the lamina pro-
pria. In one case they developed
in a solid cystic space, while in the
second case they were strictly inte-
grated in the connective tissue.
In this study, the SCTG was
obtained from the palate after ex-
traoral de-epithelialization of a
FGG under magnification by an
experienced clinician. The SCTG
is considered a highly predictable
and well-tolerated root coverage

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e250
procedure with excellent clinical
outcomes.3,4 Despite the frequency
of SCTG procedures, the number
of reports that document complica-
tions is limited.5,6 Most are related
to postoperative pain, swelling, and
bleeding; a few report reactions to
the suture materials or infection.5,6,22
There is little histologic docu-
mentation regarding SCGT com-
plications involving the gingival
connective tissue and epithelium,
and what exists is based on iso-
lated case reports.14,16,23 Occasion-
ally, a bulky tissue lesion has been
observed developing between 9
and 15 months after a SCTG or FGG
procedure.14,15,23 The excisional bi-
opsy confirmed a cyst or cystlike
formation with a stratified squa-
mous epithelial lining.14,15,23 A gingi-
val cul-de-sac with an intermittent
white discharge was also detected
3 months after a gingivoplasty car-
ried out to reduce the bulkiness of
the tissue.16
The fate of epithelial cells in-
cluded in the grafted connective
tissue is unknown. They originate
from the inclusion of epithelial rem-
nants14,15 or the invagination of the
superjacent epithelium into the
grafted connective tissue.23 Harris17
reported the presence of residual
epithelium in 80% of the grafts har-
vested from the palate in spite of at-
tempts to remove it. Nevertheless,
the grafts were successful in pro-
ducing root coverage and gingival
tissues appeared clinically healthy.17
In light of these data, it can be
hypothesized that the growth of
epithelial cells is inhibited through
a necrosis/apoptosis pathway after
being embedded under the overly-
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ing flap. Another factor to take into
account is the need for an additional
stimulus to induce epithelial tissue
to give rise to late complications.23
In the case of cysts developing after
soft tissue grafting, surgical trauma
has been proposed as the stimulat-
ing factor.16
It is also possible that during the
soft tissue healing after SCTG pro-
cedures, slight invaginations may
develop at the interface between
the CTG and the gingival flap. Histo-
logically, deep projections or down-
growths of the epithelial tissue in
the grafted connective tissue were
previously described in the litera-
ture.24,25 In the study by Ouhayoun
et al,24 these epithelial projections
were associated with an enlarge-
ment and a cystlike space in two of
the seven 12-month biopsies.24
In the present study, a solid
cyst space was located deep in
the grafted connective tissue and
no apparent epithelial invagination
connecting the cyst area with the
superficial epithelium was observed
in any of the histologic sections.
Conversely, this may be the case
for the second epithelial inclusion.
The epithelial cells were strictly inte-
grated into the lamina propria. The
boundary between epithelium and
connective tissue appeared simi-
lar to the masticatory mucosa, with
rete pegs interposed by connective
papillae. When interpreting these
histologic findings, it is important to
consider that from a clinical point of
view the size of the CTG varies ac-
cording to the individual anatomi-
cal conditions of the hard palate. A
thin masticatory mucosa increases
the likelihood of a connective tis-
sue graft being harvested with nu-
merous rete pegs.26 Thus, it may be
hypothesized that these interdigita-
tions belong to the donor site and
do not represent a secondary occur-
rence in the tissue graft as previous-
ly reported by Harris,17 who found
the presence of epithelium over a
large area in 6.7% of 30 histologi-
cally assessed SCTGs.
Since Edel27 introduced the
trap-door technique, other methods
of harvesting connective tissue from
the palate have been presented to
provide a more comfortable post-
operative period and to accelerate
the healing process.28 Nevertheless,
it is important to take into account
the palatal anatomical characteris-
tics and the thickness of the palatal
fibromucosa when selecting the ap-
propriate harvesting technique.
When the entire palatal mucosa
is at least 5 mm thick, it is possible to
harvest a CTG of proper thickness
and suitable dimensions to obtain
predictable and successful root cov-
erage. If the palatal soft tissue is not
thick enough, there is a high risk of
primary flap dehiscence/necrosis or
incorporation of fatty and glandular
tissue, inadequate for root cover-
age, when extending the dissection
deeper into the palatal tissue.7,17,28
Based on the data from the
literature reporting a mean thick-
ness of the palatal mucosa of 3.83
± 0.58 mm (range: 2.29–6.25 mm),
it can be argued that several indi-
viduals had inadequate palatal soft
tissue thickness.29 In such cases, it
is indicated to harvest a FGG and
subsequently carry out extraoral de-
epithelialization.7 This approach has
the advantage of incorporating into

the graft the most superficial por-
tion of the connective tissue, which
is denser and firmer than that closer
to the palatal bone.7 This may limit
the volumetric contraction of the
CTG during the healing phase.
A negative aspect of this de-
epithelialization technique could be
remnants of epithelium in the graft.
High magnification and proper in-
strumentation allows greater preci-
sion during surgical procedures and
decreases the risk of possible tissue
alterations of epithelial origin relat-
ed to mucogingival treatment.
In this study, the tissue cover-
ing the grafted areas appeared
clinically normal without signs of
inflammation or tumefaction. It is
unknown whether the epithelial in-
clusions would have remained as-
ymptomatic or had late clinical
manifestations. They were observed
2 months after the root coverage
procedure, whereas in the literature
all cysts or cystlike areas were as-
sociated with swelling and/or white
discharge at least 9 to 12 months
after surgery.14,16,30 It is also un-
known whether the area would have
been eliminated with time. At the
12-month follow-up, the mean per-
centage of root coverage was in line
with data in the literature.3,4
Conclusions
This study documents the possibil-
ity of early organization of epithelial
islands in the grafted tissue without
any clinical manifestations when us-
ing a SCTG obtained after the de-
epithelialization of a FGG. The fate
of epithelial cells included in the
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connective tissue is unknown. It is
possible that they give late mani-
festations that can affect root cov-
erage outcomes. Therefore, careful
removal of the covering epithelium
is necessary to increase the tissue
stability over time and to reduce the
risk of future complications of epi-
thelial origin.
Acknowledgments
The authors reported no conflicts of interest
related to this study.
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