Keratinizing Potential of
membrane coating granules.
Human Crevicular
Epithelium*
by
M . MICHAEL BRALI
S. SlGMUND STAHL ‡
T H E MORPHOLOGY of the crevicular epithelium in man
differs from that of gingival epithelium. Gingival epi­
thelium is composed of stratified squamous epithelium
normally exhibiting a keratinized or a parakeratinized
1,2
surface, while crevicular epithelium consists of a thin
layer (5-15 cells) of nonkeratinized squamous epithe­
2
l i u m . Human crevicular epithelium does not possess
either a stratum granulosum or a stratum corneum,
although these layers have been observed in the cre­
vicular epithelium of other species including the rat and
hamster. 3,4
Since morphologic appearance is a major
means of characterizing the state of keratinization of
the epithelium, it is not surprising that most theories of
keratin formation are based on the sequence of events
seen in histologic and electron microscopic prepara­
tions. The nonkeratinizing nature of human crevicular
epithelium has been reported by both light and electron
microscopic investigations. 3,7 3
M c H u g h , using polariz­
ing microscopy as well as histochemical analyses for the
distribution of sulphydryl and disulphides at the surface
of epithelium, concluded that crevicular epithelium in
man and monkey is not keratinized. In a recent ultra-
structural study of human gingiva, Takarada, et a l . ,
did not observe any discernible keratin pattern in the
crevicular epithelium and the coronal aspect of pocket
epithelium. However, some of their specimens showed
epithelia with one or more of the features associated
with the process of keratinization, i.e., keratohyaline
granules, birefringence of the spinous cells, membrane
coating granules, and thickening of the plasma mem­
brane. Although the exact role of keratohyaline gran­
ules has not been well established, recent autoradi­
ographic and biochemical data strongly suggest that
they are important precursors in the formation of the
keratin. 9,10 4
More recently, Listgarten provided further
evidence that the human crevicular epithelium has a
tendency towards keratinization. His observations were
* This paper was presented at the 55th General Session of the
International Association for Dental Research in Copenhagen, Den­
mark; March 31-April 3, 1977
†Assistant Professor, New York University College of Dentistry,
Department of Periodontics, New York, N.Y.
‡Professor and Chairman, New York University College of Den­
tistry, Department of Periodontics, New York, N . Y .
381
also supported by the appearance of keratohyaline and
Absence of keratinization has been related to the
hypothesis that nonfunctioning lining epithelium does
not keratinize in the absence of functional stimuli.
However, conversion of a nonkeratinized epit' elium to
11
a keratinized epithelium may not be related to direct
12
physical stimulation of the epithelium, but rather de­
pend on the environment in which it exists. Some
13 1 4
recent studies notably those of Innes, B a n ó c z y and
15
Caffesse and K a r r i n g have indicated that environ­
mental changes may indeed alter the keratinization
potential of crevicular epithelium. Since the nonkera­
tinized nature of the crevicular epithelium has been
considered as the "weak link" in the gingival unit, it
16-24
may serve as the site of the primary gingival l e s i o n .
Clinicians, therefore, have sought therapeutic meas­
25
ures (such as intrasulcular brushing) to enhance the
keratinization of the crevicular epithelium, thereby in­
creasing its effectiveness as a protective barrier. O n the
other hand, recent embryologic studies on epithelial-
26-30 31-33
mesenchymal interactions and grafting experi­
ments have suggested that keratinization of this tissue
may be limited by the dermal specificity of the underly­
34
ing connective tissue. Thus, therapeutic measures de­
signed to enhance keratinization would prove to be
unsuccessful.
The popularity of the concept of "connective tissue
as determinant" may be partly due to the difficulty of
designing and assessing experiments to demonstrate the
opposite. In any event, proving that connective tissue
determines epithelial morphology does not altogether
discount the possibility that epithelium also determines
connective tissue morphology, or at least, its own mor­
phology. It is this possibility that has led some workers
8
to postulate that mutual determination or an interac­
tion between both connective tissue and epithelium
35-37
may control dermal specificity. For example, A l -
38
vares and M y e r showed that there were differences
between different types of orthokeratinized epithelia,
such as that from rat cheek and rat palate, almost as
great as those between keratinized and nonkeratinized
39
epithelia. This reinforces Weinmann's suggestion that
the process of keratinization might be considered as a
spectrum, varying in small steps between the extremes
of orthokeratinization and nonkeratinization, rather
than an all-or-none process.
In order to further elucidate the keratinization po­
tential of human crevicular epithelium, we undertook a
histologic study of this epithelium when its local envi­
ronment was drastically altered.
MATERIALS A N D METHODS
A. Materials:
1. Patient Pool. Patients referred to the Periodontic
Clinic of New York University College of Dentistry
were screened for (1) motivation to take part in our

382 Bral, Stahl
study and (2) ability to effectively use oral hygiene
measures. Motivation was evaluated by interview. Oral
hygiene competence was established by the ability of
patients to remove tooth-accumulated materials suffi­
40
ciently well so that an oral hygiene index, ( O H I ) S,
approaching zero was attained. O f our patient pool,
four Caucasian female patients and one Caucasion
male patient fulfilled the above requirements and vol­
unteered for this study. These patients (a) were 23, 36,
39, 43, and 64 years old, respectively, (b) were free
from any known systemic diseases, and (c) required
gingivectomies as part of their periodontal treatment.
2. Surgical Sites. One experimental site and one
control site was utilized in each experiment. A l l surgi­
cal sites were in premolar and molar areas; four sites
were in the mandible and one in the maxilla. Four
control specimens were obtained from contralateral
sites and one specimen from the opposite jaw.
B. Methods
1. Surgical Procedures. After administration of local
anesthesia, intrasulcular mucoperiosteal flaps were re­
tracted on the facial aspects of maxillary or mandibular
premolar and molar areas. This allowed the crevicular
area to be reflected and sutured to the facial gingiva or
mucosa leaving the crevicular area exposed. A noneu-
genol dressing (Coe-pak) was placed on the surgical site
FIGURE I. A, pre-operative view of experimental site: facial gingiva in mandibular premolar and molar area. B, same site as in A,
immediately after eversion of crevicular epithelium. C, same site as in A, one week after flap eversion. Note broken suture. Much of
the crevicular surface has remained everted. D, same site as in A, four months after gingivectomy. Gingiva appears normal.
J. Periodontol.
July, 1977
and kept in position for one week. Standard methods of
pain control were prescribed. Following removal of the
dressing, sutures were maintained in place for an addi­
tional week at which point the necessary gingivectomy
was performed. Control specimens were obtained dur­
ing the patients periodontal treatment, after the healing
of the experimental sites had taken place (Fig. 1).
2. Histologic Preparations. The excised tissues were
fixed in 10% buffered neutral formalin solution,
embedded in paraffin and sectioned at 5 microns thick­
ness for histologic study. The following staining meth­
ods were utilized in serial sections:
1. Hematoxylin and eosin stain.
2. Hematoxylin-phloxin safron (HPS) stain.
3. Papanicolaou ( P A P ) stain.
4. Ayoub-Shklar method for keratin. 41
RESULTS
Clinical Observations
A. At the Time of Flap Eversion. The marginal gin­
giva of all experimental sites appeared clinically nonin-
flamed at the time of initial flap eversion. (Fig. 1 A ) .
B. One Week After Flap Eversion. Following the
eversion of the flap, no postoperative complications
occurred, nor did any of the patients need any analgesic
during the experimental period. U p o n removal of the
periodontal dressing at one week posteversion, some
Volume 48
Number 7
sutures had loosened and granulation tissue appeared
to occupy the wound site (Fig. 1C).
C . Two Weeks After Flap Eversion. A t two weeks
some sutures had been lost. However, much of the flap
remained everted in all cases. The wound surface be­
tween the teeth and the everted crevicular tissue ap­
peared to be filled with granulation tissue.
D. Postgingivectomy Healing Sequences. After gingi-
vectomy, healing was uneventful and postsurgical eval­
uation ranging from three weeks to six months postop­
eratively demonstrated normal appearing gingiva at all
surgical sites (Fig. I D ) .
Microscopic Observations
A. Control Specimens. The gingival epithelium ap­
peared fully keratinized in three specimens and para-
keratinized in the remaining two specimens.
Most crevicular epithelia exhibited either a normal
range of thickness or were slightly widened (acan­
thosis). In the latter range, the crevicular epithelium
appeared loosely knit with wider intercellular spaces.
Significant inflammatory infiltration consisting pri­
marily of lymphocytes and plasma cells was noted in the
connective tissue immediately adjacent to the crevicu­
lar epithelium. Little evidence of gingival fibers was
noted (Fig. 2).
B. Experimental Specimens. The gingival epithelium
appeared fully keratinized in two specimens and para-
keratinized in the remaining three specimens.
The crevicular epithelium exhibited a squamous cell
arrangement in all specimens. Marked acanthosis was
noted in all crevicular epithelia. Widened epithelia
ranged from 15 to 35 cell layers. The superficial layers
of the crevicular epithelium consisted of 1 to 3 cell
layers of flattened squamae, many of which were anu-
clear. The remaining cells on the surface showed pyk-
notic nuclei. Some of these cells appeared to be in the
FIGURE 2. Photomicrograph of human crevicular epithe­
lium—control specimen. Note normal thickness of nonkeratin­
ized crevicular epithelium, marked reduction of gingival fibers
in the corium and the presence of significant inflammatory
infiltrate adjacent to the epithelial surface. (H & E, magnifica­
tion x64.)
Keratinizing Potential 383
process of desquamating. A l l specimens showed kera­
tin positive staining at some or all of the surface layers
when the Papanicolaou stain or the Ayoub-Shklar
staining method were used. The coronal third of the
crevicular epithelium appeared to be parakeratinized in
all experimental specimens. A distinct basal cell layer
was noted in all experimental specimens (Figs. 3-8).
The connective tissue adjacent to the gingival epithe­
lium appeared well organized. Little evidence of in­
flammation was observed in the connective tissue im­
mediately adjacent to the crevicular epithelium. How­
ever, there seemed to be an increase in vascular chan­
nels. Collagen fibers appeared dense and well orga­
nized (Figs. 3-8).
DISCUSSION
1. Experimental Design
T o the best of our knowledge, the present study is
the first attempt to determine the keratinization poten­
tial of human crevicular epithelium by everting the
crevicular surface. Utilizing this approach, the crevicu­
lar epithelium no longer faced the tooth surface, but
rather was exposed to the oral environment.
2. Length of the Experimental Period
The decision to limit the experimental period to two
weeks was based on two considerations: (a) suture
breakage or displacement: most sutures placed on an
exposed surface either loosen or break within this time
period. This would have reduced our exposure time of
the crevicular area; and (b) our current knowledge of
the total epithelial renewal time: available human data
obtained from tritiated thymidine labeling studies indi­
cate that the renewal time of keratinized skin epithe­
42
lium is about 13 to 18 days. In a later study, this time
43
is given as 12 to 14 days. The only human study of
oral epithelium renewal time, again using tritiated thy­
midine in patients with a terminal condition, showed
that human buccal epithelium had a cell renewal rate of
44
approximately 5 days. In an attempt to compare var­
ious studies on oral epithelia of adult nonhuman pri­
45
mates, Skougaard recalculated the original data from
the literature and expressed all the results in terms of
tissue renewal or turnover time. The available data
clearly indicate that the nonkeratinizing oral epithelia
of primates turn over much faster than the keratinized
epithelia and that the turnover rate of crevicular epi­
thelium is approximately double that of gingival epithe­
lium. Thymidine labeling studies reveal a turnover time
44 46
of 4 to 8 days for the nonkeratinizing epithelia , and
7 to 15 days for the keratinizing e p i t h e l i a .16,46-48
Thus,
from both clinical and biologic observations, the two
week experimental period seemed sufficient for our
study.
 J. Periodontol.
384 Bral, Stahl July, 1977

FIGURE 3. A, Photomicrographs of human crevicular epithelium — experimental specimen from individual shown in Figure 1.
(Patient A) Hematoxylin and eosin stain. Note normal gingival epithelium with parakeratinized surface. Crevicular epithelium
shows a squamous cell arrangement. (Magnification xlO.) B, higher magnification of the crevicular area in A (arrow). Marked
acanthosis is evident in the crevicular epithelium. A striking feature is the lack of inflammatory cells in the connective tissue
immediately adjacent to the crevicular epithelium. (Magnification x25.) C, higher magnification of site from specimen in B,
demonstrating the parakeratinized features of the superficial layers of the crevicular epithelium consisting of 1-3 cells layer of
flattened squamae many of which are anuclear. Some cells show pyknotic nuclei. (Magnification xl25.)

FIGURE 4. Photomicrographs of step serial section from speci­ FIGURE 5. Photomicrographs of step serial section from speci­
men shown in Figure 3. The surface cell layers of the crevicular men shown in Figure 3. Papanicolaou stain. The surface cell
epithelium stained deep red suggestive of the presence of kera­ layers of the crevicular epithelium stained orange suggestive of
tin. Hematoxylin-phloxine safron stain. (Magnification x64.) the presence of keratin. (Magnification x64.)

3. Formation of a New Crevicular Epithelium
Following gingivectomy, a clinically normal gingival
crevice was formed. This is in accord with Listgarten's
49
study in monkeys and Innes' study in dogs which 50
showed that following gingivectomy, both the crevicu­
lar and junctional epithelia reformed at the wound
51
edge. Stahl et a l . showed similar results in their hu­
man study. The observation that following gingivec-
tomy, the stratum germinativum of the keratinized gin­
gival epithelium can give rise to distinct epithelial types
such as keratinized gingival epithelium and the crevicu­
lar epithelium, led Listgarten to suggest that "these
different epithelial types are, therefore, not genetically
predetermined, but depend more likely for their phe-
notypic expression on the environment in which they
52
exist.
Volume 48
Number 7
FIGURE 6. Photomicrographs of step serial section from speci­
men shown in Figure 3. Ayoub-Shklar staining method for
keratin. The surface cell layers of the crevicular epithelium
stained brilliant red suggestive of the presence of keratin.
(Magnification x64.)
FIGURE 7. Photomicrograph of human crevicular epithelium:
experimental specimen from Patient B demonstrating features
similar to those in Figure 3. (H & E stain. Magnification
x25.)
4. Keratinizing Potential of the Crevicular Epithelium
Our findings support the observations of Takarada et
8 4
al. and Listgarten who indicated that human crevicu­
lar epithelium has the potential to keratinize. From our
limited observations it would seem that (a) both envi­
ronmental factors and dermal specificity control the
keratinizing potential of the crevicular epithelium and,
(b) under specific circumstances (like eversion) the
environmental signal to keratinize seems greater than
the connective tissue signal to inhibit keratinization.
5. Correlation between Inflammation and Keratinization
A striking feature in our experimental specimens was
the lack of inflammation in the connective tissue adja­
cent to the crevicular epithelium. This is contrary to the
universally reported presence of inflammatory cells in
the connective tissue of the crevicular wall in human
53
gingival specimens. It has been suggested that the
gingival inflammatory infiltrate may be the response to
either irritation from bacterial plaque entering the con­
Keratinizing Potential 385
FIGURE 8. Photomicrograph of human crevicular epithelium:
experimental specimen from patient C demonstrating features
similar to those in Figures 3 and 7. (H & E stain. Magnifica­
tion x64.)
54
nective tissue, or as part of an immunopathologic
55, 5 6
mechanism, or both. It is significant that gingival
inflammation is not normally seen in young rodents
whose crevicular epithelium is well keratinized, while
in man gingival inflammation is extremely common in
57
adolescents and young adults. The striking lack of
inflammation in our experimental specimens may be
due to (a) physical separation of the crevicular tissue
from direct contact with the bacterial plaque, or (b) the
possible mechanical stimulation of the crevicular epi­
thelium during the experimental period by either rub­
bing against the surgical dressing or brushing. The
effects of mechanical stimulation on increased keratini­
58-64
zation has been well-documented.
65,66
It is our belief that it was the physical s e p a r a t i o n
of the crevicular tissue from bacterial plaque which
resulted in the reduction of inflammation. This, in turn,
may have allowed the keratinization potential of the
crevicular epithelium to express itself. Such a sequence
would be in accord with the general biologic data sug­
gesting that all epithelia have the potential to keratin­
4, 8 , 3 8 , 3 9
ize. Therefore, it would seem that our initial
experiments may well serve as an introduction to fur­
ther studies regarding the influence of local irritants on
the inhibition of crevicular keratinization. Such infor­
mation would aid our biologic approach to the treat­
ment of periodontal disease.
SUMMARY
The effects of environmental changes on the keratin­
ization potential of human crevicular epithelium were
evaluated histologically in five adults undergoing peri­
odontal treatment. With patient consent, surgery was
scheduled only when optimum oral hygiene was at­
tained. Under local anesthesia an intrasulcular muco-
periosteal flap was retracted on the facial aspect of
selected sites. This allowed the crevicular area to be
reflected and sutured to the facial gingiva or mucosa,
leaving the crevicular epithelium exposed. A noneu-

386 Bral, Stahl
genol dressing was placed on the surgical site for one
week. Following removal of dressing, sutures were
maintained in place for an additional week at which
time gingivectomy was performed. Tissues excised at
other gingivectomy sites in the same patients were used
as controls. Specimens were prepared for histologic
study and special stains were used to determine kera­
tinization patterns. Healing was uneventful. Histologi­
cally, cells at the everted crevicular epithelium showed
evidence of parakeratinization. In addition, a marked
acanthosis was noted. O f further interest was the mini­
mal inflammation seen in the connective tissue adjacent
to the everted crevicular epithelium, whereas signifi­
cant inflammation was present in all control specimens.
Our observations suggest that environmental
changes such as physical separation of crevicular tissues
from the tooth and its adherent plaque may enhance
the keratinization potential of crevicular epithelium in
association with a reduction in local inflammation.
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Number 7 Keratinizing Potential 387

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Announcement
UNIVERSITY OF SOUTHERN CALIFORNIA SCHOOL OF
DENTISTRY
The University of Southern California, School of Dentistry an­
nounces the following graduate dentistry courses:
TITLE: Graduate Programs
DATE: July, 1978
FACULTY: JOHN C. VINTON, P H . D . , Director of Admissions, Uni­
versity of Southern California, School of Dentistry
Applications may be obtained for advanced training in Endodon­
tics, Orthodontics, Pedodontics, Periodontics, Prosthodontics, Oral
Pathology and Oral Surgery. Each program commences July 1. The
Hospital residency programs are available in advanced Pedodontics
and Oral Pathology which provide monthly stipends. For additional
information, contact the University of Southern California, School of
Dentistry, Office of Admissions, 925 West 34th Street, Los Angeles,
Calif 90007.