Jan Lindhe. Clinical Periodontology

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ALVEOLAR BONE FORMATION • 887

The technique advocated involves a combined split-

thickness/full-thickness mucoperiosteal flap extend-

ing between the teeth adjacent to the defect. Care is

taken to place the initial incision over intact bone

remote from the bone defect. No vertical releasing

incisions are placed, but the incisions extend into the

gingival sulcus of the neighboring teeth.

Following flap elevation, soft tissue within the de-

fect is carefully removed (Fig. 38-34a). A barrier mem

brane is adjusted and adapted to cover the bony defect

and 3-4 mm of the surrounding intact bone, but avoid

ing contact with the adjacent teeth (Fig. 38-34c). In

situations where there is a possible risk of collapse of

the membrane barrier into the defect, miniscrews

(

MemfiO, Straumann Institute, Waldenburg, Switzer-

land) are placed to support the membrane for mainte

nance of the secluded space created (Fig. 38-34b).

Cortical bone lining the defect is perforated into the

subjacent cancellous bone (Fig. 38-34b). The mucope-

riosteal flaps are subsequently repositioned and

tightly sutured with mattress sutures. Postsurgical

plaque control includes two daily rinsings with a

chlorhexidine solution. Care is exercised not to touch

or press the surgical site while using temporary recon

structions. The sutures are removed after 14 days.

Postsurgical visits at monthly intervals to check the

course of healing and the patient's plaque control are

advocated (Fig. 39-34d). The removal of the mem-

branes is performed 6-8 months after surgery (Fig.

38-34e).

In the case of exposure of the membrane prior to the

scheduled removal, special efforts have to be made to

prevent infection of the treated area by using antimi-

crobial therapy. At the time of membrane removal, the

volume of newly formed bone corresponds to ap-

proximately 90-100% of the space created by the bar-

rier membrane. Occasionally, a soft tissue coverage

most likely originating from the bone marrow is seen

888 • CHAPTER 38

Fig. 38-34. Alveolar ridge augmentation. (a) Bony defect (156 m

) in the maxilla of a 45-year-old woman follow

ing flap elevation. (b) Mini-supporting screws placed for the support and fixation of a membrane. (c) Placement of

fixation-screws to adapt the membrane. (d) Soft tissue healing of the augmented ridge prior to membrane removal.

(e) Regenerated bone under the membrane at the time of removal 8 months postsurgically. Effective new bone vol

ume: 144 m

, or 92% of the space volume. (f) Appearance of a thin, dense layer of nonmineralized tissue

located

between the regenerated bone surface and the inner surface of the membrane.

under the membrane (Fig. 38-34f). This well-vascular-

ized connective tissue forms a periosteal envelope

along the bone surface (Schenk et al. 1994). Provided

an undisturbed healing of 6-8 months is observed,

remarkable volumes of new alveolar bone may be

generated by the GTR principle, resulting in an ade-

quate volume for implant placement. Using this tech-

nique a clinical study of 40 partially edentulous pa-

tients was presented (Buser et al. 1996a,b). The pa-

tients who were admitted consecutively to the study

had 66 augmented sites which were used for implant

placement 7-13 months following the augmentation

of the alveolar crest. All but one patient showed com-

plication-free soft tissue healing with an enlargement

of the crest width ranging from 3.5 mm to 7.1 mm. The

outcome of the procedure allowed the placement of a

non-submerged titanium implant in all situations.

Another retrospective study (Lang et al. 1994b) util-

izing the same technique also confirmed a 6-8-month

period of undisturbed healing as a prerequisite for a

successful treatment outcome. Between 90% and 100%

of the volume created by the membrane was filled

with

regenerated bone after this time, while a shorter

undisturbed healing period (3-5 months) yielded a

ALVEOLAR BONE FORMATION •

889

Fig. 38-35. Alveolar bone dehiscence exposing the

threads of an implant.

Fig. 38-36. Alveolar bone fenestration exposing an im

plant buccally.

regenerated volume of unpredictable magnitude (0-

60%). Infection after membrane exposure was the ma

jor source of complication. A publication (Buser et al.

1996a,b), presenting 5-year results of the first group of

12 patients with alveolar ridge enlargement, has docu

mented the long-term stability of the results.

Alveolar bone dehiscences and fenestrations

in association with oral implants

An implant dehiscence is defined as exposure of the

implant surface from the top of the implant head to

the point where the implant is totally covered by bone

(

Fig. 38-35). An implant fenestration or window of

exposed implant surface results from either insuffi-

cient buccolingual alveolar width or inadvertent mis-

direction of implant placement (Fig. 38-36).

Jovanovic et al. (1993) evaluated the potential for

bone regeneration at dehisced dental implant sites in

a clinical study including 11 patients. Nineteen tita-

nium dental implants with exposed threads were

studied. In order to create a secluded space for bone

formation, a barrier membrane was placed over the

exposed implant sites and secured with an implant

cover screw. Subsequently the implants were com-

pletely covered with the surgical flaps. Clinical evalu-

ation of the treatment was performed 4

/2-6 months

after initial surgery. Fourteen out of 19 dehisced im-

plant sites revealed 100% bone fill of the space created

by the membrane. In addition, alveolar ridge augmen

tation had occurred at these sites. However, in cases

where the membrane and the implant were exposed,

minimal bone regeneration occurred. Six to 12 months

after prosthesis connection, 12 of the 19 implants were

available for radiographic analysis, and an average

bone loss of 1.73 mm was measured.

In a prospective multicenter study (Dahlin et al.

1995), implant dehiscences and fenestrations were

evaluated 3 years following alveolar bone augmenta-

tion therapy. Out of 54 augmented sites, six mem-

branes were exposed and four implants were lost at

the time of abutment connection, corresponding to an

implant failure rate of 7.4% after 1 year. The cumula-

tive survival rates after 2 years were 85% and 95% for

the maxilla and the mandible, respectively. At 3 years,

the rates decreased to 76% and 83%, respectively.

These rates are clearly lower than those regularly

reported for implant placement into a bone volume of

sufficient dimension. Hence, it has to be considered

that augmenting bone at exposed implant threads

may involve additional risk factors for the longevity

the implants placed.

Immediate implant placement following

tooth extraction

Placement of implants at the time of tooth extraction

is called "immediate implant placement".

Several authors have reported placement of im-

plants into extraction sockets and augmentation of

these sites with barrier membranes (Lazzara 1989,

Becker & Becker 1990, Nyman et al. 1990). The ration

ale for this procedure is to decrease the restorative

time, to promote bone-to-implant contact and to pre-

serve

eolar bone height. Indications for extraction

and immediate implant placement are: failed endo-

dontically-treated teeth, teeth with advanced peri-

odontal disease, root fractures and advanced caries

beneath the gingival margin. However, teeth with

suppuration or large periapical infections are not can

didates for extraction and immediate replacement

with implants. A prospective clinical multicenter

study (Becker et al. 1994) evaluated implants which

were placed into extraction sockets and augmented by

GTR. Out of 49 implants, three were lost prior to

loading. These implants had premature membrane

exposure. At 3 years, 93.9% of the implants remained

functional. Bone formation adjacent to the implants

was related to barrier membrane retention. Sites

where the barrier remained unexposed had greater

amounts of bone fill in the sockets (average of 4.8 mm)

when compared with sites where the membranes be-

came prematurely exposed and were removed (aver-

age of 4.0 mm). Recently, 109 Nobel Biocare implants

890 • CHAPTER 38

Fig. 38-37. (a) Root fracture following trauma of tooth 11. (b) Extraction socket 11 following careful removal of the

tooth after raising a flap. (c) Preparation of the implant bed into the palatal socket wall. (d) Considerable lack of

bone on the buccal aspect. (e) Barrier membrane shaped and adapted around the neck of the hollow cylinder im

plant demonstrating primary stability. (f) Single interrupted sutures mesial and distal to the implant. (g) The mem

brane has been

in situ

for 6 months. Infection was prevented by chemical plaque control. A flap was raised and the

membrane removed from the soft and underlying hard tissue. (h) Radiographic appearance of new bone generated

underneath the membrane after 10 years. The entire plasma-sprayed surface of the implant is still covered with

bone. (i) Final reconstruction: porcelain fused to metal crown seated 7 months after the tooth extraction and main

tained for 6 years.

immediately placed into extraction sockets were

evaluated up to 5

years (average 2

years) follow-

ing the treatment (Rosenquist & Grenthe 1996). The

survival rate was 94% and the success rate 92%. Even

though implants immediately placed into extraction

sockets have been reported to have predictable heal-

ing in a

submerged

environment, the

non-submerged

placement of an implant into an extraction socket

would offer a number of advantages. A series of

methodologic reports and clinical studies evaluated the

healing of immediate one-stage transmucosal im-

plants (Cochran & Douglas 1993, Lang et al. 1994a,

Tritten et al. 1995, Bragger et al. 1996, Hammerle et al.

1998).

One prospective study (Lang et al. 1994a) on the

installation of immediate transmucosal implants in

combination with GTR evaluated 21 implants in 16

patients after 2

years. By meticulous antimicrobial

ALVEOLAR BONE FORMATION •

891

Fig. 38-37, g-i.

prophylactic procedures, including regular and pro-

longed topical use of antiseptics in conjunction with

postsurgical administration of antibiotics, membrane

removal was generally performed after 6 months.

With the exception of one implant, complete fill of the

extraction socket was achieved without the use of any

autogenous or heterologous filler materials.

Another study on 10 patients with re-entry after 6

months following the placement of one-stage trans-

mucosal implants into extraction sockets revealed a

mean filling-up of 6.7 mm of the bone missing at the

extraction sites, which corresponded to 94% of the

volume estimates of bone fill at these sites (Hammerle

et al. 1997). Most of these studies were performed

using non-resorbable occlusive barrier membranes to

cover the self-containing defects at the extraction sites.

However, bio-resorbable collagen barriers in conjunc-

tion with the application of deproteinized bone min-

eral as a supporting material also resulted in predict-

able treatment outcomes (Hammerle & Lang 2001).

When compared to the standard placement of

transmucosal implants, immediate transmucosal im-

plants yielded very similar favorable clinical condi-

tions in both groups of patients in a cross-sectional

study after 1 year (Bragger et al. 1996). Low plaque

and mucositis indices, similar amounts of recession,

probing pocket depths and clinical attachment levels

were registered in 41 patients.

In summary, five determining factors were identi-

fied to be prerequisites for positive treatment out-

comes in the placement of

one-stage non-submerged

implants placed

immediately

into extraction sockets:

Preservation of the bony margins of the alveolus

during extraction to provide the necessary support

for the barrier membrane.

Primary implant stability by precise preparation of

an implant bed in the apical portion or along the

walls of the socket.

Tight circumferential adaptation of a barrier mem-

brane as a collar around the neck of the implant

extending over the borders of the alveolus by 3-4

mm.

Careful management of the soft tissue flap and

close flap adaptation to the neck of the implant. If

the latter cannot be achieved, the extraction socket

should be left to heal for 1 month to obtain a soft

tissue coverage of the wound. The implant may

then be placed into this recent extraction site (Wil-

son & Weber 1993).

Meticulous plaque control for the entire healing

period of approximately 6 months. This is achieved

by postsurgical antibiotic coverage, daily oral

rinses

with chlorhexidine and daily application of

chlorhexidine gel under the base of the temporary

restoration.

A clinical situation in which tooth 11 was lost owing

to a long fracture (Fig. 38-37a) may illustrate the clini

cal procedure. A mucoperiosteal flap is raised on both

the buccal and oral aspects ranging from tooth 13 to

892 • CHAPTER 38

Fig. 38-38. An osseous submucous

cleft palate is produced surgically

(a). A membrane is placed both on

the nasal (b) and palatal aspects

tissue flap is repositioned and su

tured (d).

tooth 21. Tooth 11 is carefully extracted using fine

elevators and small desmosomes to avoid the break-

age of the buccal bony plate (Fig. 38-37b). If present,

granulation tissue is removed. Immediately following

the extraction and after rinsing the socket with sterile

saline, an implant bed is prepared at the bottom or into

the walls of the sockets (Fig. 38-37c) to obtain primary

stability by intimate bone-to-implant contact (Fig. 38-

37d).

In order to obtain bone fill of the circumferential

defects adjacent to the implant and osseointegration

also in the coronal part of the exposed plasma-sprayed

implant surface, a barrier membrane is individually

adapted to surround the neck of the implant tightly

and to cover the bony defect around the implant (Fig.

38-37e). Care is taken to extend the barrier membrane

3-4 mm beyond the bony edges of the defect. Also, any

contact of the membrane material with the adjacent

teeth is avoided. Subsequently, the soft tissue flap is

adapted snugly around the collar of the implants,

allowing for transmucosal integration of these one-

stage implants. Individual interrupted sutures are

placed (Fig. 38-37f).

To prevent colonization with microorganisms lead-

ing to infection in the wound area, the patients should

receive systemic antibiotics (amoxicillin) for 5-10

days. In addition, the patients should rinse twice daily

with a chlorhexidine solution for at least 3 weeks after

placement of the implants. A 1% chlorhexidine gel

may be applied topically twice daily from the time of

surgery and until the prosthetic appliance is incorpo-

rated. Since GTR may require longer periods of undis

turbed healing for bone than for periodontal ligament

regeneration (Lang et al. 1994a), the barrier membrane

is intended to be left for periods of at least 6-8 months.

During this healing phase, the patients are checked

once a month for plaque removal. During the healing

period, the implants are functionally not loaded, i.e.

the patients are provided with temporary removable

partial dentures with no contact between the base of

the denture and the soft tissue surrounding the imme

diate implants. The barrier membrane is removed

under local anesthesia (Fig. 38-37g). The newly gener

ated bone adjacent to the implant may be seen. Fol-

lowing resuturing, the flap adapting the soft tissues

around the neck of the implant at the site is allowed

to heal for 2-3 weeks. Subsequently, the final recon-

struction is installed. After 6 years the radiographic

documentation demonstrates stability of the bone

level (Fig. 38-37h) and the peri-implant mucosal tis-

sues are clinically healthy (Fig. 38-37i).

PERSPECTIVES IN BONE

REGENERATION WITH GTR

In the studies described above, jaw bone defects in rats

and monkeys healed with complete bone fill when

covered with Teflon" membranes, whereas soft tissue

invaded control defects treated without membranes

(

Dahlin et al. 1988, 1989, Kostopoulos & Karring

1994a,b). This observation suggests that GTR can be

applied successfully in the field of cranio- and maxil-

lofacial surgery. In fact, a study (Matzen et al. 1996)

has demonstrated that healing of osseous submucous

cleft palate defects with bone can be achieved by GTR.

Osseous submucous cleft palate defects were pro-

duced surgically in rats (Fig. 38-38a). Barrier mem-

branes were placed so that they covered both the nasal

ALVEOLAR BONE FORMATION •

Fig. 38-39. (a) Microphotograph showing a membrane (M)-covered defect completely filled with new bone with a

suture-like tissue (arrow) in the middle. (b) Control defect invaded by soft tissue.

Fig. 38-40. A segmental, 1-cm osteoperiosteal defect

produced in the radius of a rabbit and subsequently

covered with a bioabsorbable membrane.

Fig. 38-41. Radiograph (a) and microphotograph (b) of a control defect treated without a membrane. The defect dis

plays a characteristic non-union with rounded bone ends (arrows) separated by soft tissue.

(Fig. 38-38b) and the palatal (Fig. 38-38c) aspect of the

defect before the raised palatal mucoperiosteal flap was

repositioned and sutured (Fig. 39-38d). Histologic and

macroscopic examination of defleshed specimens

showed that complete healing of the defects with a

suture-like tissue in the middle (Fig. 38-39a) was ac-

complished in all the membrane-treated defects, while

soft tissue had invaded the control defects treated

without a membrane (Fig. 38-39b).

There are also reasons to believe that the principle

of GTR can be successfully applied in orthopedic sur-

gery. This view is based on the results of studies in

rabbits in which healing of long bone segmental de-

fects was accomplished by connecting the bone frag-

ments with a bioabsorbable membrane tube (Nielsen

1992, Nielsen et al. 1992). Segmental 1-cm osteope-

riosteal defects were produced in both radii of rabbits.

One defect was covered with a bioabsorbable mem-

brane (Fig. 38-40), while the contralateral defect with-

out a membrane served as control. Nine out of 10

control defects displayed non-union (Fig. 38-41),

whereas all membrane-treated defects healed by a

callus external to the membrane, producing continu-

ity between the bone fragments. However, loose con-

nective tissue was predominant in the gap underneath

the membrane. When, in a second experiment, demin-

894 • CHAPTER 38

Fig. 38-42. Radiograph (a) and microphotograph (b) of a test defect treated with a membrane (M) and the place-

ment of demineralized bone in the defect. The defect displays osseous continuity with the formation of a cortical (

C) bone cylinder surrounding a marrow canal (MC). A narrow zone of woven bone with a central transverse disk

cartilagenous tissue remains in the midportion of the defect (arrows).

eralized bone matrix (DMB) was placed in the gap

inside the tube, all membrane-covered defects exhib-

ited osseous continuity with the formation of a cortical

bone cylinder surrounding a marrow canal inside the

tube (Fig. 38-42a).

A narrow midline zone of woven bone with a cen

tral

transverse disk of cartilaginous tissue remained in

some

of the covered defects after 12 weeks (Fig. 38-

42b). Histologic examination of this zone revealed that

bone formation resembling endochondral ossification

at growth plates was taking place in this area. These

observations suggest that the combined use of GTR

and DMB may have a clinical application in the treat-

ment of large bony defects in long-bone fractures and

in bone-lengthening procedures.

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