Jan Lindhe. Clinical Periodontology

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MUCOSITIS AND PERI-IMPLANTITIS • 1017

Fig. 44-3. (a) A clinical view describing features of experimental peri-implantitis in the beagle dog. (b) A clinical

view describing features of experimental periodontitis in the beagle dog.

and in the monkey (Lang et al. 1993, Schou et al. 1993).

Although the experiments had somewhat varying de-

sign, the outcome of the studies was almost identical

and, hence, only the result from the dog model will be

reported.

In the

dog model,

the premolars were extracted in

one side of the mandible, fixtures (Branemark sys-

tems) were inserted and abutment connection per-

formed 3 months later as described above (Berglundh

et al. 1991). During the healing phase a strict plaque

control regimen was maintained and healthy tissue

conditions were hereby established in all tooth and

implant sites to be monitored.

On a given day, the periodontitis and peri-implan-

titis lesions were induced. This was accomplished by

(

1) terminating the plaque control regimen, and (2)

placing cotton floss ligatures around the neck of both

the premolar teeth and the implants. The ligatures

were forced into a position apical of the soft tissue

margins. A "pocket" between the tooth/gingiva and

implant/mucosa was thereby created, a submarginal

microbiota rapidly formed and inflammatory lesions

developed in the neighboring tissues. Radiographs

obtained after 6 weeks of experiment revealed that a

substantial amount of bone tissue had been lost at both

teeth and implant sites. The ligatures were removed.

After another 4 weeks, the animals were re-examined

(

Fig. 44-3a,b), radiographs obtained, bacteria sampled

and biopsies of tooth and implant sites harvested.

It was observed that the plaque that had formed in

the deep "pockets" was similar at tooth and implant

sites and was dominated by Gram-negative and an-

aerobic species (Leonhardt et al. 1992). This observa-

tion is consistent with findings indicating that in hu-

mans, the microbiota at teeth and implants has many

features in common but also that the microbiota at

healthy and diseased sites — tooth sites as well as

implant sites — is very different. Thus, implants and

teeth that are surrounded by healthy soft tissues are

associated with biofilms including small amounts of

Gram-positive coccoid cells and rods. Sites with exten-

sive periodontal and peri-implant inflammation har-

Fig. 44-4. Microphotograph (buccal/lingual section) il

lustrating the periodontitis lesion. Note the apical ex-

tension of the infiltrate (arrow) but also the presence of

a zone of normal connective tissue between the infil-

trate and the bone crest (arrow).

bor biofilms with large numbers of Gram-negative

anaerobic bacteria (for review see Mombelli 1999).

The histopathologic examination of the biopsy

samples from the dog study (Lindhe et al. 1992) re-

vealed that there were marked differences in the size

and location of the inflammatory lesions of the two

sites. Thus, while the lesions in the periodontal sites

(

Fig. 44-4) were consistently separated from the alveo-

lar bone by a zone, about 1 mm high, of non-inflamed

connective tissue, the lesion in the peri-implant tissue

in most situations extended into and involved the

marrow spaces of the alveolar bone.

It was concluded that the pattern of spread of in-

flammation was different in periodontal and peri-im-

plant tissues. The lesions in plaque-associated perio-

dontitis were limited to the connective tissue, while in

the peri-implant tissues the lesions involved, in addi-

1018 •

CHAPTER 44

Fig. 44-5. (a) Ground section illus

trating a peri-implantitis lesion.

The implant is positioned to the

left and the apical portions of the

infiltrate (arrows) extend into con

-tact with the bone. (b) Close up

of (a) illustrating the presence of

inflammatory cells and

osteoclasts (arrow) on the bone

surface.

Fig. 44-6. Microphotograph illus-

trating a human peri-implantitis

lesion. Note the large inflamma-

tory infiltrate lateral to the pocket

epithelium (a). The implant was

positioned to the left. Arrows indi

cate vascular units illustrated in a

larger magnification in (b).

tion, the alveolar bone (Fig. 44-5a,b). It was suggested

that the peri-implant tissues, in variance with the

periodontal tissues, are poorly organized to resolve

progressive, plaque-associated lesions. In subsequent

studies (Marinello et al. 1995, Ericsson et al 1996,

Persson et al. 1996, Gotfredsen et al. 2002), using simi

lar models but allowing for different periods of tissue

breakdown, the validity of this conclusion was sub-

stantiated.

Histopathologic analyses of tissues sampled from

peri-implantitis sites in humans revealed the presence

of large inflammatory cell infiltrates in the mucosa.

Sanz et al. (1991) analyzed soft tissue biopsies from six

patients with peri-implantitis and reported that 65%

of the connective tissue portion was occupied by an

inflammatory cell infiltrate. Piattelli et al. (1998) de-

scribed histopathologic characteristics of tissues from

230 retrieved implants. It was reported that at sites

where implants were removed due to peri-implantitis,

"an inflammatory infiltrate, composed of macro-

phages, lymphocytes and plasma-cells, was found in

the connective tissue around the implants". In a study

on human peri-implantitis lesions, Berglundh et al. (

2003) found that the mucosa contained large lesions

with numerous plasma cells, lymphocytes and macro-

phages (Fig. 44-6a,b). It was further demonstrated that

the inflammatory cell infiltrate consistently extended

to an area apical of the pocket epithelium and that the

apical part of the soft lesion frequently reached the

bone tissue. Berglundh et al. (2003) also observed that

numerous PMN cells were present in the human peri-

implantitis lesion. Such cells occurred not only in the

pocket epithelium and associated areas of the lesions,

but also in peri-vascular compartments distant from

the implant surface. Further, in the apical part of the

lesion the inflamed connective tissue appeared to be

in direct contact with the biofilm on the implant sur-

face. Gualini & Berglundh (2003) used immunohisto-

chemical techniques to analyze the composition of

lesions occurring in the peri-implant mucosa sampled

MUCOSITIS AND PERI-IMPLANTITIS • 1019

Fig. 44-7. Clinical (a) and radiographic (b) characteristics of two implant sites with peri-implantitis in the left side

of the mandible. Note the presence of swelling and suppuration in the peri-implant mucosa (a) and the crater

formed bone destruction around the implants in the radiograph (arrows) (b).

Fig. 44-8. Clinical and radiographic characteristics of the two implant sites illustrated in Fig. 42-7 at 6 months after

treatment. Note the recession of the peri-implant mucosa (a) and the altered outline of the peri-implant bone (b).

from sites with peri-implantitis in six volunteers. The

elastase marker, indicating PMN cells, was found in a

large number of cells in the central portions of the

infiltrate. This finding indicates a high PMN cell ac-

tivity at sites with peri-implantitis and is in agreement

with observations made by Hultin et al. (2002). They

analyzed crevicular fluid that was sampled from im-

plant sites in 17 patients with peri-implantitis and in

19 patients with "stable marginal tissue conditions".

The authors found that sites with peri-implantitis had

higher elastase activity and concentration of lactofer-

rin than control sites.

The findings described above — large numbers of

neutrophils in the peri-implantitis lesion and the ab-

sence of an epithelial lining between the lesion and the

biofilm — indicate that the peri-implantitis lesions have

features that are different from those of perio

dontitis

lesions.

Conclusion

Peri-implantitis lesions are poorly encapsulated, ex-

tend into the marginal bone tissue and may, if they are

allowed to progress, lead to the loss of the implant.

Symptoms of peri-implantitis relate to the infec-

tious/inflammatory nature of the lesion. Thus, there

is radiographic evidence of bone loss and the bone loss

consistently takes the shape of a crater. Swelling and

redness of the mucosa as well as bleeding on gentle

probing and suppuration frequently occur. The im-

plant may remain stable over long periods.

TREATMENT OF PERI-IMPLANT

TISSUE INFLAMMATION

Resolution of the inflammatory lesion

In dog experiments by Ericsson et al (1996) and Pers-

son et al. (1996, 1999), peri-implantitis lesions were

first produced according to the technique previously

described (Lindhe et al. 1992). The peri-implantitis

lesions were subsequently exposed to therapy. Thus,

antibiotics (amoxicillin and metronidazole) were ad-

ministered via the systemic route to the animals but

local treatment was provided to only some of the

diseased implant sites. Following several months of

healing, it was observed that in implant sites also

given local therapy, i.e. submarginal debridment, the

1020 • CHAPTER 44

inflammatory lesions were resolved. In implant sites

not exposed to local debridement, however, the in-

flammatory infiltrate in the mucosa as well as in the

bone tissue persisted.

These observations clearly demonstrate that a treat-

ment regimen that is restricted to systemic administra-

tion of antibiotics is not effective in the management

of peri-implantitis, but must always be combined with

meticulous removal of the biofilm from the contami-

nated implant surface.

In this context it must be remembered that in the

treatment of chronic periodontitis administration of

systemic antibiotics but no local therapy (i.e. scaling

and root planning) is an improper regimen. It will fail

to resolve the inflammatory lesion in the gingiva and

fail to arrest the further progression of tissue break-

down (Lindhe et al. 1983a,b, Berglundh et al. 1998).

Re-osseointegration

In the animal experiments it was noted that even

though a combined systemic and local antimicrobial

therapy successfully resolved the inflammatory le-

sion, this regimen failed to promote "re-osseointegra-

tion", i.e. the formation of new bone in contact with

the previously contaminated titanium surface. It is

likely that the biofilm that formed on the implant

during the tissue breakdown phase altered the surface

characteristics of the titanium body. It is well known

that pristine implants made of commercially pure

titanium are covered with a thin layer of titanium

dioxide. This dioxide layer gives the implant a high

surface energy that facilitates the interaction between

the implant and the cells of the host tissues (Bair &

Meyer 1988). Contamination of a titanium surface,

however, markedly alters its characteristics. An im-

plant with a low surface energy results. Such a surface

may not allow tissue integration to occur but rather

provokes a foreign body reaction (Bair & Meyer 1988,

Sennerby & Lekholm 1993).

Different techniques have been proposed for a local

therapy aimed at "re-juvenating" a once contami-

nated implant surface. Such techniques have included

mechanical brushing of the surface, the use of air-

powder abrasives, the application of chemicals such

as citric acid, chlorhexidine and delmopinol (Persson

et al. 1999, Wetzel et al. 1999). These local therapies

were effective in cleaning the titanium surface and to

allow soft tissue healing and bone fill in the defects,

but only limited amounts of re-osseointegration oc-

curred.

The techniques described above regarding treat-

ment of peri-implantitis lesions including systemic

antibiotics and local therapy (debridement and re-

moval of granulation tissue) are apparently effective

and have been utilized also in humans. Fig. 44-7a,b

shows two implant sites with peri-implantitis in the

left side of the mandible. The clinical and radiographic

characteristics of the two implant sites at 6 months

after treatment (antibiotics and local therapy) are pre-

sented in Fig. 44-Sa,b. The recession of the peri-im-

plant mucosa is evident and probing at the two sites

did not result in bleeding (a). Note the altered outline

of the peri-implant bone in (b).

Conclusion

Current knowledge has documented that the use of

antibacterial treatment procedures will effectively re-

solve the inflammatory component of the peri-im-

plantitis lesions. Re-osseointegration to a once con-

taminated implant surface is difficult and the outcome

of such regenerative procedures is difficult to predict.

MICROBIAL ASPECTS ASSOCIATED

WITH IMPLANTS IN HUMANS

Microbial colonization

Successful implants

Biofilms consist of highly organized microcolonies of

bacteria within a glycocalyx matrix. They form on all

hard, non-shedding surfaces situated within an aque-

ous environment. Thus, a biofilm will readily form on

the portion of an implant exposed to the oral cavity.

The microbial colonization of titanium implants has

been studied in humans using microscopy, culture

techniques and DNA analysis.

Mombelli et al. (1988) investigated the early coloni-

zation of titanium implants placed in edentulous

mandibles. The composition of the biofilm associated

with healthy peri-implant tissues was established

within 7 days of implantation. It consisted of mainly

Gram-positive facultatively anaerobic rods and cocci,

and showed no shifts in composition over time.

Gram–negative anaerobic rods accounted for only a

small proportion of the microflora. This microbiologi-

cal profile associated with successful implants is simi-

lar to that found at periodontally healthy teeth and has

been confirmed by others (Apse et al. 1989, Bower et

al. 1989, Mombelli & Mericske-Stern 1990, Sordyl et al.

1995).

Peri-implant infections

The composition of the microflora associated with

peri-implant infection is markedly different to that

associated with successful implants. In overview,

there is a transition from small quantities of plaque,

predominantly Gram-positive cocci, with low propor-

tions of Gram-negative species, to a larger amount of

plaque with increased proportions of Gram-negative

anaerobic and facultative anaerobic species (Rams &

Link 1983, Rams et al. 1984, Mombelli et al. 1987,

Alcoforado et al. 1991, George et al. 1994, Augthun &

Conrads 1997, Salcetti et al. 1997). The microflora

associated with peri-implantitis is similar to that asso-

MUCOSITIS AND PERI-IMPLANTITIS • 1021

dated with periodontal disease. Opportunistic peri-

odontal pathogens such as

Actinobacillus actinomy-

cetetncomitans, Porphyromonas gingivalis, Bacteroides

forsythus, Prevotella intermedia, Peptostreptcoccus micros

and

Fusobacterium nucleatum

have been identified in

association with peri-implantitis in partially edentu-

lous patients (van Winkelhoff & Wolf 2000, van

Winkelhoff et al. 2000).

In addition, microorganisms primarily not associ-

ated with periodontitis, such as

Staphylococcus

spp.,

enterics and

Candida

spp., have also been suggested to

play a role in peri-implantitis (Rams et al. 1990, Alco

forado et al. 1991, Rosenberg et al. 1991, Leonhardt

et al. 1999, Kronstrom et al. 2001).

There is evidence that potential pathogens identi-

fied around remaining teeth may colonize implants

within 6 months of placement of implants (Apse et al.

1989, Quirynen & Listgarten 1990, Koka et al. 1993,

Leonhardt et al. 1993, Kohavi et al. 1994, Mombelli et

al. 1995, van Winkelhoff et al. 2000). Proliferation of

these opportunistic pathogens results in an inflamma-

tory response and may lead to peri-implant infection.

This emphasizes the importance of the establishment

of healthy periodontal conditions prior to placement

of implants in partially edentulous patients, and the

importance of a regular maintenance program there-

after.

Treatment of peri-implant infection

The goal of therapy is the suppression of the oppor-

tunistic pathogens associated with the infection, and

the establishment of a local environment and mi-

croflora compatible with health. Treatment should

begin with an infection control program including

oral hygiene instruction, mechanical debridement

and removal of the biofilm within the peri-implant

pocket, and the regular application of an antimicrobial

agent such as chlorhexidine gel or mouthrinse. In

most cases of peri-implant mucositis this infection

control regimen will be sufficient to reduce the quan-

tity of plaque and to establish a microflora associated

with healthy peri-implant tissues.

Additional treatment for peri-implantitis may in-

clude the use of adjunctive antibiotic therapy, either

systemically or locally administered (see CIST proto-

col, Chapter 45). As is the case in periodontal therapy,

antibiotics used alone are ineffective. The nature of a

biofilm affords protection to its co-inhabitants, and

they may develop resistance to antimicrobial agents

via a number of mechanisms. Therefore, antibiotics

should always be prescribed in conjunction with dis-

ruption of the biofilm by mechanical debridement.

Furthermore, a microbiological diagnosis may be of

value for guidance in the choice of antimicrobial treat-

ment for patients with peri-implant infection.

There are only two studies monitoring the changes

in the microflora following treatment of peri-implan-

titis in humans. Mombelli & Lang (1992) observed a

reduction in the quantity and proportions of anaerobic

bacteria following systemic administration of ornida-

zole, an antibiotic that specifically targets Gram-nega-

tive anaerobic organisms. The alteration in the micro-

bial composition was accompanied by a sustained

clinical improvement over a 1-year period.

In the second study, peri-implantitis treatment us-

ing local delivery of tetracycline demonstrated a posi-

tive effect on clinical and microbiological parameters (

Mombelli et al. 2001). The local delivery device Ac-

tisite® (fibers containing polymeric tetracycline HCl)

resulted in significantly lower total anaerobic bacte-

rial counts than at baseline. A significant decrease in

frequency of detection was observed for

Prevotella

intermedia/nigrescens, Fusobacterium

sp.,

Bacteroides

forsythus,

and

Campylobacter rectus.

In order for a local delivery device to be effective

against the microorganisms within a biofilm, the ac-

tive agent must reach the peri-implant pocket in suf-

ficient concentration for a long enough time. Thus the

kinetics of the local delivery device are critical. A

number of local antibiotic therapies are currently

available; however, the tetracycline fibers are, to date,

the only local delivery device evaluated for the treat-

ment of peri-implantitis (see Chapter 45).

Conclusion

Bacteria play a major role in the etiology of peri-im-

plant mucositis and peri-implantitis. There are dis-

tinct differences in the microflora associated with suc-

cessful implants and implants with peri-implantitis.

Remaining teeth with periodontal disease may pro-

vide a reservoir for colonization of implants by oppor-

tunistic periodontal pathogens. Periodontal health

should therefore be achieved prior to implant place-

ment. Treatment of peri-implant infection aims at sup-

pression of the Gram-negative anaerobic bacteria and

the establishment of a local environment and mi-

croflora conducive to peri-implant health.

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1022 • CHAPTER 44

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CHAPTER 45

Maintenance of the

Implant Patient

NIKLAUS P. LANG AND JAN LINDHE

Goals

The diagnostic process

Bleeding on probing

Suppuration

Probing depth

Radiographic interpretation

Mobility

Cumulative Interceptive Supportive Therapy

(

CIST)

Preventive and therapeutic strategies

Since their introduction in the 1970s, endosseous oral

implants have become an integral part of reconstruc-

tive dentistry. Initially, implant therapy was predomi-

nantly intended for the fully edentulous patient. In

recent years, however, the partially dentate patient

has also become a candidate for implant placement. In

such a patient, both dental and implant abutments are

used to reconstruct the compromised dentition. This

blend of teeth and implants is, in particular, critical in

the periodontally susceptible patient in whom the

submarginal biofilms may harbor putative periodon-

tal pathogens which may also be involved in the

processes associated with the resorption of the bony

support for the implant.

The objective of this chapter is to describe the pre-

vention and therapy of problems around implants

that arise from microbial colonization on teeth and

implants in the periodontally susceptible patient.

GOALS

Inflammatory lesions occurring in the peri-implant

tissues were described in Chapter 44. Such processes

are the result of opportunistic infections and may, if

left untreated, progress deep into the supporting bone

and lead to implant loss. It is, therefore, imperative

that the tissues around implants be monitored at regu

lar intervals to discover arising biological complica-

tions and to interfere with the disease process at an

early stage. The appropriate therapy instituted fol-

lowing the diagnosis must be aimed towards the re-

duction of the submucosal biofilm and the alteration

of the ecological conditions for the bacterial habitat.

THE DIAGNOSTIC PROCESS

The examination of the tissues around implants has

many features in common with the periodontal ex-

amination (Chapter 18) and must include parameters

relevant to the pathogenic process of the peri-implant

infection. It should be understood that, while ad-

vanced peri-implant lesions are easily recognized on

radiographs, early alterations in the mucosa are often

site specific and discrete. Hence, they require for their

detection a systematic examination that should in-

clude assessments of:

•

Bleeding on probing (BoP)

•

Suppuration

•

Probing depth (PPD)

•

Radiographic bone loss

• Implant mobility.

Assessments of BoP, suppuration and PPD must be

made at four surfaces (mesial, buccal, distal and lin-

gual) of each implant, while radiographic interpreta-

tion is limited to the evaluation of the mesial and distal

aspects.

MAINTENANCE OF THE IMPLANT PATIENT • 1025

Fig.

45-1.

Suppuration in combination with the devel-

opment of a fistula indicates clinical signs of active peri-

implant infection.

Bleeding on probing (BoP)

Bleeding on probing (BoP+) occurring following the

application of the probe with a light pressure (0.25 N)

reveals the presence of an inflammatory lesion in the

gingiva around teeth (Lang et al. 1991). Although this

symptom (BoP+) may have a limited predictive value

for periodontal disease progression (Lang et al. 1986),

its absence (BoP—) indicates periodontal stability (

Lang et al. 1990). With regard to the mucosa around

implants, the diagnostic accuracy of BoP appears to be

even better than that of BoP in a periodontal examina-

tion (Luterbacher et al. 2000). Hence, a peri-implant

site that following probing is BoP negative is consid-

ered healthy and stable.

Suppuration

As indicated in Chapter 44, peri-implant infections are

characterized by inflammatory processes that contain

a variety of leukocytes. In the inflammatory lesions

collagen is destroyed and tissue necrosis results. This

process leads to pus formation, suppuration and the

development of a fistula (Fig. 45-1). Hence, suppura-

tion must be associated with episodes of active tissue

destruction and indicates a need for anti-infective

therapy.

Probing depth

As stated in Chapter 35, probing in the peri-implant

sulcus must be made with a light probing force (about

0.2-0.3 N) to avoid undue tissue damage and overex-

tension into the healthy tissues (Mombelli et al. 1997).

If a light probing pressure is applied during prob-

ing, the epithelial attachment of the transmucosal tis-

sue seal will be disrupted but will heal within 5-7 days

(Etter et al. 2002). This means that — as is the case in

probing around teeth (Taylor & Campbell 1972) —

probing the peri-implant tissue can be performed

Fig.

45-2.

Clinical probing of the peri-implant sulcus re

sults in complete epithelial attachment after

5-7

days,

thus not damaging the transmucosal soft tissue seal.

From Etter et al.

2002.

without causing permanent damage to the integrity of

the transmucosal attachment.

Clinical probing must thus be regarded as an im-

portant and reliable diagnostic parameter in the con-

tinuous monitoring of both periodontal and peri-im-

plant tissues (Fig. 45-2).

The diagnostic value of probing the mucosa around

implants was also described in Chapter 35. Thus, at

sites with healthy mucosa or mucositis, the tip of the

probe may identify the location of the apical level of

the barrier epithelium (Ericsson & Lindhe 1993, Lang

et al. 1994). Since the barrier epithelium is about 2-3

mm long, the probing depth at such sites should be 5

3 mm. At sites with peri-implantitis, however, the

probe will penetrate apical to the epithelium and reach

the base of the inflammatory lesion at the alveolar

bone crest (Lang et al. 1994). Consequently, an in-

creased probing depth will result.

Radiographic interpretation

The preservation of marginal bone height is crucial for

implant maintenance and is often used as a primary

success criterion for different implant systems. A

mean marginal bone loss amounting to less than 0.2

mm annually following the first year of service was

originally proposed as one of the major success criteria

(Albrektsson et al. 1986, Lekholm et al. 1986). This

success criterion has been questioned, since recent

longitudinal studies have demonstrated that loss of

alveolar bone may be almost absent or minimal in

well-maintained patients.

In this context, it is important to realize that in the

individual patient, a mean alveolar bone loss/year

may be a misleading parameter, since peri-implant

1026 • CHAPTER 45

Fig. 45-3. Peri-implantitis resulting in the loss of an old titanium implant after 8 years of function. (a) Loss of alveo

lar bone and peri-implant lesion progressing into the implant concavity. Clinical signs of advanced peri-implant in

fection. (b) Explanted implant of (a) affected by peri-implantitis. Active infective lesion in the coronal part of the im

plant (granulation tissue: red, bacterial colonization: brown) and perfect osseointegration in the apical part (alveo

lar bone: green). (c) Cross-sectional ground section through the apical portion of the explanted implant from (a) in

dicating perfect osseointegration. As a consequence, the implant remains clinically stable. Hence, mobility repre

sents a diagnostic test with poor sensitivity

infections are implant specific. Hence, in a given pa-

tient the mean bone loss may be small, but one of

multiple implant sites may be severely affected and in

need of anti-infective therapy. Radiographic interpre-

tation should not be the only parameter to estimate

the

performance of implants. In the absence of clinical

signs of infection, it is recommended to take radio-

graphs 1 year after implant installation and no more

than every other year thereafter (Chapter 36). Addi-

tional radiographs may be obtained to determine the

extent of marginal bone loss if clinical parameters (e.g.

BoP+, suppuration, and increased probing depth) in-

dicate peri-implant infection.

Mobility

Implant mobility indicates lack of osseointegration.

Even if peri-implantitis has progressed relatively far,

implants may still appear clinically stable due to some

remaining direct bone to implant contact (Fig. 45-

3a,

b,c). Mobility, therefore, is a specific diagnostic test

for

loss of osseointegration and is decisive in the decision

to remove the affected implant.

CUMULATIVE INTERCEPTIVE

SUPPORTIVE THERAPY (CIST)

Preventive and therapeutic strategies

Depending on the clinical, and eventually the radio-

graphic diagnosis, protocols for preventive and thera-

peutic measures were designed to intercept the devel-

opment of peri-implant lesions. This system of sup-

portive therapy is cumulative in nature and includes

four steps which should not be used as single proce-

dures, but rather as a sequence of therapeutic proce-