Jan Lindhe. Clinical Periodontology

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SURFACE TOPOGRAPHY OF TITANIUM IMPLANTS • 827

Fig. 34-12. A TiUnite

flank,

where

the oxidation process has

resulted in

a lot of pores. The po

rous structure

will increase the

surface area more

than other sur

faces with similar

average height deviation. Each

section of the red

and white bars

represents a length

of 10 .tm.

Fig. 34-13. Bonefit'

, a titanium

plasma sprayed surface with a

rough structure. Some parts of

this

area are rather smooth, others

very

rough. Each section of the

red and

white bars represents a

length of

10 µm.

Fig. 34-14. A turned implant flank

with marks from the cutting proce-

dure clearly visible. Each section

the red and white bars represents a

length of 10 µm.

828 •

CHAPTER 34

Titanium

plasma sprayed surface Turned surface

(Bonefit

, Institute Straumann AG, Waldenburg, (MKIII

, Nobel Biocare, Goteborg, Sweden.) Cutting

Switzerland.) Plasma spraying results in a rough but marks from the machining process result in an ori-

still

isotropic surface. The surface of the implants was ented anisotropic surface. The surface of the implants

found

to have an average height deviation of 2.35 tm had an average height deviation of 0.71 tm (S

), an

average wavelength of 13.15 µm (S

) and an average wavelength of 9.84 pm (S

) and an increased

increased surface area of 87% (S

). (Fig.34-13).

surface area of 19% (S

) (Fig.34-14).

(SteriOss

, Replace system, Nobel Biocare, US.) The MK III implants had a rougher surface com-

This was

the roughest implant surface among those pared to the turned "coronal part" of the Osseotite

measured.

The implant surface was found to have an implant. The average height deviation was for

average height

deviation of 3.86 µm (S

), an average Osseotite "coronal part", 0.53 µm, and the average

wavelength of 19.55

µm (S

) and an increased surface wavelength and developed surface area was 8.6 tm

area of 134% (S

and 15%, respectively.

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Clinical Oral

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11-19.

CHAPTER 35

The Transmucosal Attachment

JAN LINDHE AND TORD BERGLUNDH

Normal peri-implant mucosa

Probing gingiva and peri-implant mucosa

Dimensions

Composition

Vascular supply

The wound healing that occurs following the closure

of mucoperiosteal flaps during implant surgery re-

sults in the establishment of a mucosal attachment

(

transmucosal attachment) to the implant. The trans-

mucosal attachment serves as a seal that prevents

products from the oral cavity reaching the bone tissue

that anchors the implant.

NORMAL PERI-IMPLANT

MUCOSA

Dimensions

The structure and function of the mucosa that sur-

rounds implants made of commercially pure (c.p.)

titanium has been examined in man and several ani-

mal models (for review see Berglundh 1999). In an

early study in the dog, Berglundh et al. (1991) com-

pared some anatomical features of the gingiva (at

teeth) and the mucosa at implants. Since the research

protocol from this study was used in subsequent ex-

periments that will be described in this chapter, details

regarding the protocol are briefly outlined here.

The mandibular premolars in one side of the man-

dible were extracted, leaving the teeth in the contralat

eral jaw quadrant. After 3 months of healing following

tooth extraction (Fig. 35-1) implants (i.e. the fixture

part; Fig. 35-2; Branemark System

, Nobel Biocare,

Gothenburg, Sweden) made of c.p. titanium were in-

stalled according to the guidelines given in the man-

ual for the system. Another 3 months later, abutment

connection was performed (Fig. 35-3) in a second-

stage procedure and the animals were placed in a

careful plaque control program. This called for tooth

and implant cleaning five times a week. Four months

Fig. 35-1. The edentulous mandibular right premolar re

gion 3 months following tooth extraction (from Ber-

glundh et al. 1991).

Fig. 35-2. Three titanium implants (i.e. the fixture part

and cover screw; Branemark Syste

) are installed.

subsequent to abutment connection, the dogs were

exposed to a clinical examination following which

biopsies of several tooth and all implant sites were

harvested.

The clinically healthy gingiva and peri-implant

830 • CHAPTER 35

Fig. 35-3. Abutment connection is performed and the

mucosa sutured with interrupted sutures.

mucosa had a pink color and a firm consistency (Figs.

35-4a,b). In radiographs obtained from the tooth sites

it was observed that the alveolar bone crest was lo-

cated about 1 mm apical of a line connecting the

cemento-enamel junction of neighboring premolars

(

Fig. 35-5a). The radiographs from the implant sites

disclosed that the marginal termination of the bone

crest was close to the junction between the abutment

and fixture part of the implant system (Fig. 35-5b).

The histologic examination of the sections (pre-

pared in a buccal-lingual direction) revealed that the

two soft tissue units, the gingiva and the peri-implant

mucosa, have several features in common. The oral

epithelium of the gingiva is well keratinized and is

continuous with a smooth junctional epithelium that

faces the crown of the tooth and ends at the cemento

enamel junction (arrow) (Fig. 35-6). The supra-alveo-

lar connective tissue is about 1 mm high (arrows) and

the periodontal ligament about 0.2-0.3 mm wide. The

principal fibers extend from the root cementum in a

fan-shaped pattern into the soft and hard tissues of the

marginal periodontium (arrows; Fig. 35-7).

The outer surface of the peri-implant mucosa is also

covered by a well-keratinized oral epithelium, which

in the marginal border (arrow) connects with a barrier

epithelium that is facing the abutment part of the

implant (Fig. 35-8). This barrier epithelium has several

features in common with the junctional epithelium

found on the tooth site. The barrier epithelium is only

a few cell layers thick (Fig. 35-9) and terminates about

2 mm apical of the soft tissue margin (arrows; Fig.

35-

8). In a zone that is about 1-1.5 mm high, between

the

apical level of the barrier epithelium and the al

veolar

bone crest, the connective tissue appears to be

in direct

contact with the TiO

layer of the implant

(Figs. 35-8,

35-10). The collagen fibers seem to origi

nate from the

periosteum of the bone crest and extend

towards the

margin of the soft tissue in directions

parallel to the

surface of the abutment.

The observation that the barrier epithelium – dur-

Fig. 35-4. After 4 months of careful plaque control the gingiva (a) and the peri-implant mucosa (b) are clinically

healthy.

Fig. 35-5. Radiographs obtained from the premolars in the left side (a) and from the implants in the right side of the

mandible (b).

THE TRANSMUCOSAL ATTACHMENT • 831

Fig. 35-6. Microphotograph of a cross-section of the

buccal and coronal part of the periodontium of a

mandibular premolar. Note the position of the soft tis-

sue margin (top arrow), the apical cells of the junc-

tional epithelium (center arrow) and the crest of the al-

veolar bone (bottom arrow). The junctional epithelium

is about 2 mm long and the supracrestal connective tis

sue portion about 1 mm high.

Fig. 35-7. Higher magnification of the supracresta con

nective tissue portion seen in Fig. 35-6. Note the direc

tion of the principal fibers (arrows).

Fig. 35-8. Microphotograph of a buccal/lingual section

Fig. 35-9. Higher magnification of the apical portion of

of the peri-implant mucosa. Note the position of thethe barrier epithelium (arrow) in Fig. 35-8.

soft tissue margin (top arrow), the apical cells of the

junctional epithelium (center arrow) and the crest of

the marginal bone (bottom arrow). The junctional epi-

thelium is about 2 mm long and the implant/connec-

tive tissue interface about 1.5 mm high.

ing healing following the abutment connection proce- connected. The severed connective tissue parts of the

dure –

consistently ends at a certain distance from the mucosa are placed in contact with the abutment. The

bone is

important. During the surgical procedure an process of healing starts and in the "apical" parts of

incision is made

in the ridge mucosa, the marginal the abutment an interaction must occur between the

portion of the fixture is identified and the abutment is

connective tissue and the TiO

layer of the metal de-

832 • CHAPTER 35

Fig. 35-10. Microphotograph of a section (buccal/lin-

gual) of the implant/connective tissue interface of the

peri-implant mucosa. The collagen fibers invest in the

periosteum of the bone and project in directions paral

lel to the implant surface towards the margin of the

soft tissue.

vice. This zone of interaction is apparently not recog-

nized as a wound and therefore does not call for an

epithelial lining.

Summary

The junctional and barrier epithelia are about 2 mm

long and the zones of supra-alveolar connective tissue

are between 1 and 1.5 mm high. Both epithelia are via

hemi-desmosomes attached to the tooth/implant sur-

face (Gould et al.

1984).

The main attachment fibers

(

the principal fibers) invest in the root cementum of

the

tooth, but at the implant site the corresponding

Fig. 35-11. Implants of three systems installed in the

mandible of a beagle dog. Astra Tech Implant

Dental

System (left), Branemark System

(center) and ITI

Dental Implant System (right).

fibers apparently originate from the periosteum of the

adjacent bone crest.

In further dog experiments of similar design (Abra-

hamsson et al.

1996, 2001) it was observed that identi-

cal transmucosal attachment features occurred when

different types of implant systems were used (e.g. Astra

Tech Implants

, Dental system, Molndal, Swe

den;

Branemark System

, Nobel Biocare, Gothenburg,

Sweden; ITI

Dental Implant System, Straumann AG,

Waldenburg, Switzerland; 3i

Implant System, Im-

plant Innovation Inc., West Palm Beach, FL, US) and

also independent of whether the implant was initially

submerged.

The clinical characteristics of the peri-implant mu-

cosa that occurred with three different implant sys-

tems (Astra Tech, Branemark and ITI systems) are

presented in Fig. 35-11. The Astra Tech and the Brane

mark implants were initially submerged and abut-

ments installed in a second surgical procedure, while

Fig. 35-12. Microphotographs illustrating the mucosa (buccal/lingual view) facing the three implant systems: (a)

Astra, (b) Branemark and (c) ITI.

THE TRANSMUCOSAL ATTACHMENT •

Fig. 35-13. Schematic drawing illustrating that the mu

cosa at the test site was reduced to about 2 mm.

the ITI implant was placed in a one-stage procedure.

The geometry of the transmucosal part of the implants

varied considerably from one system to the next. Fig.

35-12 presents microphotographs documenting the

transmucosal soft tissue attachment of the three im-

plant systems. Note that in all three sites examined:

•

the profile of the implant is recorded in the adjacent

tissue

•

the transmucosal attachment is comprised of one

barrier epithelium (about 2 mm) and one zone of

connective tissue attachment (about 1-1.5 mm

high)

In another study using the same model (Abrahamsson

et al. 1996), it was demonstrated that the material used

in the abutment part of the implant was of decisive

importance for the quality of the attachment that oc-

curred between the abutment and the surrounding

mucosa. Thus, abutments made of aluminum-based

sintered ceramic (Al

) allowed for the establ

ishment

of a mucosal attachment similar to that which

occurred

at titanium implants. Abutments made of

gold alloy or

dental porcelain provided inferior mu

cosal healing.

Thus, to abutments made of such mate

rials a zone of

connective tissue attachment failed to

develop. The

mucosal attachment occurred instead in

a more apical

location, i.e. at the fixture level. Thus,

during healing

following abutment connection some

resorption of the

marginal bone must occur to "open" the titanium

portion (i.e. the fixture) of the implant for

the

formation of a connective tissue attachment.

The biological height of the transmucosal attach-

ment was further examined in a dog experiment by

Berglundh & Lindhe (1996). All mandibular premo

lars

were first removed and the extraction sites al-

lowed to

heal for several months after which implants

(fixtures)

of the Branemark System

were installed

and

submerged. After 3 months of healing, abutment

connection was performed. In the left side of the man-

dible the volume of the ridge mucosa was maintained

while in the right jaw the vertical dimension of the

mucosa was reduced to <_ 2 mm (Fig. 35-13). In biopsies

obtained after 6 months of careful plaque control, it

Fig. 35-14. Schematic drawing illustrating that the peri

implant mucosa at both control and test sites contained

a 2 mm long barrier epithelium and a zone of connec-

tive tissue that was about 1.3-1.8 mm high. Bone resorp

tion occurred in order to accommodate the soft tissue

attachment at sites with a thin mucosa.

Fig. 35-15. Microphotograph illustrating the peri-im-

plant mucosa of a normal dimension (left) and reduced

dimension (right). Note the angular bone loss that had

occurred at the site with the thin mucosa.

was observed that the transmucosal attachment at all

implants included one barrier epithelium that was 2

mm long and one zone of connective tissue attach-

ment that was 1-1.5 mm high.

A further examination of the peri-implant tissues at

sites where the mucosa prior to abutment connection

was made thin ( 2 mm), disclosed that wound healing

consistently had included marginal bone resorption to

establish a mucosa that was 3 mm high. In this

context it must be realized that the connective tissue

attachment at such sites occurred not at the abutment

but at the fixture level (Figs. 35-14, 35-15).

Conclusion

The transmucosal attachment that occurs at implants

made of c.p. titanium is comprised of two parts: one

834 • CHAPTER 35

Fig. 35-16. (a) Microphotograph of

a tooth with marginal periodontal

tissues (buccal/lingual section).

Note on the tooth side the pres-

ence of an acellular root cemen-

tum with inserting collagen fibers.

The fibers are orientated more or

less perpendicular to the root sur-

face. (b) Microphotograph of the

peri-implant mucosa and the bone

at the tissue/titanium interface.

Note that the orientation of the

collagen fibers is more or less par-

allel (not perpendicular) to the ti-

tanium surface.

Fig. 35-17. Schematic drawing illustrating the two

zones in the implant/connective tissue interface. Zone

A (40

µm

wide) is located next to the implant surface,

while zone B (160 µm wide) resides lateral to zone A.

Fig. 35-18. Microphotograph of the implant/connective

tissue interface of the peri-implant mucosa. A large

number of fibroblasts reside in the tissue next to the im

plant.

barrier epithelium that has features in common with a

junctional epithelium and is about 2 mm long. This

barrier epithelium is continuous with one zone of

connective tissue, about 1-1.5 mm high, that attaches

("integrates") to the implant and contains collagen

fiber

bundles, some of which invest in the periosteum

of the

bone crest and run a course parallel with the

surface of

the implant.

Composition

The quality, i.e. the composition, of the connective

tissue in the supra-alveolar compartments at teeth and

implants was examined by Berglundh et al. (1991).

The authors stated that the main difference between

the mesenchymal tissue present at a tooth and at an

implant site is the occurrence of a cementum (acellular

or cellular) on the root surface. From this, often-acel-

lular extrinsic fiber cementum (Fig. 35-16a), coarse

dento-gingival and dento-alveolar collagen fiber bun-

dles project in lateral, coronal and apical directions

(

Fig. 35-7).

At the implant site, the collagen fiber bundles are

orientated in a completely different manner. Thus, the

fibers invest in the periosteum at the bone crest and

either project in directions parallel with the implant

surface (Fig. 35-16b), or aligned as coarse bundles

which — in areas distant from the implant — run a

course more or less perpendicular to the implant sur-

face. These "horizontal fibers" appear to bend in a

vertical" direction, i.e. become parallel with the im

plant

surface, in compartments close to the implant

(Buser

et al. 1992).

The connective tissue in the attachment zone at

implants contains more collagen, but fewer fibroblasts

and vascular structures, than the tissue in the corre-

sponding location at teeth. A more detailed analysis of

the composition of the connective tissue in the

attachment zone at implants (made of c.p. titanium)

THE TRANSMUCOSAL ATTACHMENT •

835

Fig. 35-19. Abuccal/lingual section

of a beagle dog gingiva. Cleared sec-

tion. The vessels have been filled

with carbon. Note the presence of a

supraperiosteal vessel on the out-

side the alveolar bone, the presence

of a plexus of vessels within the

periodontal ligament, as well as vas-

cular structures in the very mar-

ginal portion of the gingiva.

Fig. 35-20. (a) A buccal/lingual cleared section of a beagle dog mucosa fac

ing an implant (the implant was positioned to the right). Note the

presence

of a supraperiosteal vessel on the outside of the alveolar bone,

but also that

there is no vasculature that corresponds to the periodontal

ligament plexus.

(b) Higher magnification (of a) of the peri-implant soft

tissue and the bone

implant interface. Note the presence of a vascular

plexus lateral to the junc

tional epithelium, but the absence of vessels in

the more apical portions of

the soft tissue facing the implant and the

bone.

was made by Moon et al. (1999) in a dog experiment.

They reported that this border tissue could be divided

into two zones: zone A and zone B (Fig. 35-17). Zone

is about 40 tm wide and resides next to the implant

surface. In this zone there are virtually no blood ves-

sels but a large number of fibroblasts that are orien-

tated with their long axes parallel with the implant

surface (Fig. 35-18) (collagen 67%, vascular structures

0.3% and fibroblasts 32%). In zone B – that in lateral

direction is continuous with zone A and is 160 µm

wide – there are fewer fibroblasts but more collagen

fibers and more vascular structures (collagen 85%,

vascular structures 3% and fibroblasts 11%). Abra-

hamsson et al. (2002) analyzed the connective tissue

attachment at implant abutments with different sur-

face roughness in dogs. It was reported (1) that the

composition of the connective tissue facing the differ-

ent surfaces was virtually similar, and (2) that the

cell-

rich interface portion was comprised of round

and flat-

shaped fibroblasts. From these findings it

may be

concluded that the attachment between the

TiO

layer

on the titanium surface and the connective tissue is

maintained, and if damaged is repaired, by

cellular (

fibroblast) activity.

Vascular supply

The vascular supply to the gingiva comes from two

different sources (Fig. 35-19). The first source is the

large

supraperiosteal blood vessels,

which put forth

branches to form (1) the capillaries of the connective

tissue papillae under the oral epithelium and (2) the

vascular plexus lateral to the junctional epithelium.

The second source is the

vascular plexus of the periodon-

tal ligament,

from which branches run in a coronal

direction, pass the alveolar bone crest and terminate

the supra-alveolar portion of the free gingiva. It is,

thus, important to realize that the blood supply to the

zone of connective tissue attachment in the periodon-

tium is derived from two apparently independent

sources (see also Chapter 1).

Berglundh et al. (1994) observed that the vascular

system of the peri-implant mucosa of dogs (Fig. 35-

20a,b) originated

solely

from the large

supraperiosteal

blood vessel

on the outside of the alveolar ridge. This

vessel gives off branches to the supra-alveolar mucosa

and forms (1) the capillaries beneath the oral epithe-

lium and (2) a vascular plexus located immediately

lateral to the barrier epithelium. Further, the implant

site lacks a periodontal ligament, and consequently

the

site also lacks a vascular plexus in the interface

between the bone and the titanium surface. As a con-

sequence, the connective tissue part of the transmu-

cosal attachment to titanium implants contains only a

few vessels, all of which are terminal branches of the

supraperiosteal blood vessels.

Conclusion

The gingiva at teeth and the mucosa at implants made

836 • CHAPTER 35

Fig. 35-21. Clinical photograph illustrating the position

of the periodontal probes which via a cementing sub-

stance were attached to the tooth and the implant sur

face.

Fig. 35-22. Schematic drawing illustrating the probe in

position at the tooth site and at the implant site. Note

that at the tooth site the probe fails to reach the apical

cells of the junctional epithelium, and that the gingiva

becomes compressed in apical direction. On the im-

plant site, the probe passes beyond the apical cells of

the junctional epithelium. Note also that the peri-im-

plant mucosa during probing is displaced mainly in

the lateral direction.

of titanium have some characteristics in common, but

differ in the composition of the connective tissue, the

alignment of the collagen fiber bundles and the distri-

bution of vascular structures in the compartment api-

cal of the barrier epithelium.

PROBING GINGIVA AND

PERI-IMPLANT MUCOSA

It has been demonstrated in several studies (see Chap

ter 18) that the tip of a periodontal probe in a "pocket

depth" measurement at a

tooth site

seldom identifies

the apical termination of the dentogingival epithe-

lium. Thus, the junctional epithelium offers no resis-

tance to the probe. If an inflammatory lesion – rich in

leukocytes and poor in collagen – is present in the

gingival connective tissue, the probe may penetrate

beyond the apical termination of the epithelium and

reach the apical-lateral border of the infiltrate. In the

absence of an inflammatory lesion, e.g. following suc-

cessful therapy, however, the probe frequently fails to

reach the apical part of the junctional epithelium.

The outcome of probing depth measurements at

implant sites

was examined in the beagle dog model by

Ericsson & Lindhe (1993) and Lang et al. (1994) and in

monkeys

(Macaca fascicularis)

by Schou et al (2002).

Ericsson & Lindhe (1993) used the model by Ber-

glundh et al. (1991) referred to above and, hence, had

both teeth and implants available for examination.

The gingiva at mandibular premolars and the mucosa

at correspondingly positioned implants (Branemark

System

) were, after extended periods of plaque con-

trol, considered clinically healthy. A probe with a tip

diameter of 0.5 mm was inserted into the buccal

pocket" using a standardized force of 0.5 N (Fig.

35-21).

The probe was anchored to the tooth or to the implant

and biopsies from the various sites were har

vested.

The histologic examination of the biopsy ma

terial

revealed that probing the dento-gingival inter-face had

resulted in a slight compression of the gingi

val tissue.

The resulting "histologic" probing depth was 0.7 mm.

The tip of the probe was located coronal to the apical

cells of the junctional epithelium (Fig.

35-22). At the

implant sites, probing caused both com

pression and a

lateral dislocation of the peri-implant

mucosa, and the

average "histologic" probing depth

was markedly

deeper than at the tooth site, namely 2.0

mm. The tip of

the probe was consistently positioned

deep in the

connective tissue/abutment interface and

apical of the

barrier epithelium. The distance between

the probe tip

and the bone crest at the tooth sites was

about 1.2

mm. The corresponding distance at the im

plant site

was 0.2 mm. This means that at the implant

sites, the

probe almost made contact with the bone

crest. From

these observations, it may be concluded

that the

attachment between the implant surface and

the

mucosa was weaker than the corresponding at-

tachment between the tooth and the gingiva, and that

care must be exercised when data from probing depth

measurements from tooth and implant sites are com-

pared.

Lang et al. (1994) used five beagle dogs and pre-