Jan Lindhe. Clinical Periodontology

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27.

CHAPTER 5

Host-Parasite Interactions in

Periodontal Disease

DENIS F. KINANE, TORD BERGLUNDH AND JAN LINDHE

Initiation and progression of periodontal

disease

Introduction

Initiation of periodontal disease

hlitial, early, established and advanced lesions

Host-parasite interactions

Introduction

Microbial virulence factors

Host defense processes

Overall summary

INITIATION AND PROGRESSION OF

PERIODONTAL DISEASE

Introduction

Current concepts regarding the etiology and patho-

genesis of periodontal disease are derived mainly

from the results of epidemiological studies, analyses

of autopsy and biopsy material, clinical trials and

animal experimentation. Findings from epidemiologi-

cal studies have consistently revealed that the experi-

ence and extent of periodontal disease increases with

age and with inadequate oral hygiene (see Chapter 3).

Studies on the extent and severity of periodontal dis-

ease involvement have changed our view on the

prevalence and progression of destructive periodon-

tal disease. Relatively few subjects in each age group

suffer from advanced periodontal destruction and

these few subjects account for most of the sites which

are severely periodontally involved (Loe et al. 1986,

Papapanou et al. 1988, Yoneyama et al. 1988, Jenkins

& Kinane, 1989). hl addition, longitudinal studies us-

ing large thresholds for declaring disease detection

have shown that relatively few sites undergo exten-

sive periodontal destruction within a given observa-

tion period and these are found in only a small subset

of the population (Haffajee et al. 1983a,b, Lindhe et al.

1983, Jenkins et al. 1988). Socransky et al. (1984) sug

gested that periodontitis progresses in episodes of

exacerbation and remission (the burst hypothesis).

More recent studies have suggested that the progres-

sion may be more continuous than episodic and that

detection of "bursts" may be due to an inadequate

resolution of clinical measurements (Jeffcoat & Reddy

1991).

• In summary, periodontal disease is subject related;

only a few individuals experience advanced de-

struction affecting several teeth; and the progres-

sion of the disease is probably continuous with brief

episodes of localized exacerbation and remission.

Initiation of periodontal disease

Most normal subjects maintaining a high standard of

oral hygiene are not likely to develop advanced peri-

odontal disease. Experimental, short-term clinical

studies have shown that microorganisms quickly start

to colonize clean tooth surfaces once an individual

abstains from mechanical tooth cleaning; within a few

days microscopical and clinical signs of gingivitis are

then apparent. These inflammatory alterations are re-

solved or reversed when adequate tooth-cleaning

measures are resumed (Loe et al. 1965). Thus, micro-

organisms which form the dental biofilm contain or

release components which induce gingivitis. Consis-

tent with this conclusion is the finding that topical

applications of soluble plaque extracts produce in-

flammatory alterations in gingival tissues (Hellden &

Lindhe 1973). Long-term clinical trials have under-

lined the importance of removing the subgingival

biofilm in order to successfully treat periodontal dis-

ease in humans (Ramfjord et al. 1968, Lindhe & Ny-

man 1975, 1984, Axelsson & Lindhe 1978, 1981).

Furthermore, animal experiments (especially in

HOST-PARASITE INTERACTIONS IN PERIODONTAL DISEASE • 151

Fig. 5-1. (a) Overview of a buccal-lingual section of a normal (pristine) beagle dog gingiva. The oral epithelium (

OE) is continuous with the junctional epithelium GE), which is facing the enamel surface. CT = connective tissue;

CEJ = cemento-enamel junction. (b) Detail of 5-1a. The oral epithelium is continuous with a thin junctional epithe-

lium. Note the presence of neutrophils in the outer portion of the junctional epithelium. (c) The junctional epithe-

lium is only 10-15 cell layers thick and permeable for bacterial products. (d) Micrograph of a buccal-lingual

section of a normal (pristine) beagle dog gingiva illustrating the vasculature of the gingival unit. A thin vascular

network is present beneath the junctional epithelium. (e) The thin vascular network (plexus) is shown in a mesial-

distal section.

dogs and non-human primates) have confirmed the

infectious etiology of gingival/periodontal lesions.

Long-term observations in beagles, for example, indi-

cate that gingivitis develops only in animals that ac-

cumulate plaque. The inflammatory changes may re-

main confined to the gingival area for several years,

but at some sites gingivitis eventually shifts to de-

structive periodontal disease resulting in loss of con-

nective tissue attachment and alveolar bone (Saxe et

al. 1967, Lindhe et al. 1975).

It is implied that most forms of periodontal disease

are plaque-associated disorders which start as an overt

inflammation of the gingiva. If left untreated, in

certain susceptible individuals, inflammation may

spread to involve deeper portions of the periodontium.

It is not presently understood why, in some patients,

lesions remain localized to the marginal portion of the

gingival tissues, whilst in others they progress to

involve the loss of connective tissue attachment and

supporting alveolar bone. The same arguments are

true for individual sites within a susceptible individual.

Clearly some imbalance of the host-microbial

relationship is occurring in the destructive lesions,

which may be unique to that site and to periodontally

susceptible individuals generally.

152 • CHAPTER 5

Fig. 5-2. (a) Microphotograph of a buccal-lingual section of a normal beagle dog gingiva. A filter paper-strip has

been introduced between the junctional epithelium and the tooth. An increased permeability of the gingival vessels

has occurred. The increased vascular permeability is in this case identified by the presence of carbon particles

which prior to biopsy were injected intravenously. The carbon particles have become trapped in the open endothe

lial junctions, and so-called vascular labelling has occurred. (b) A mesio-distal section of the same gingival unit

as in Fig. 5-2a. (c) Higher magnification of Fig. 5-2b (from Egelberg 1967).

Normal

"clinically

healthy"

gingiva and

"experimental gingivitis"

Normal gingiva is characterized clinically by its pink

color and firm consistency and the gingival margin

exhibits a scalloped outline. The interdental papillae

are firm, do not bleed on gentle probing and fill the

space below the contact areas. The gingiva often ex-

hibits a stippled appearance and there is a knife edge

margin between tooth and soft tissue. Normal gingi-

vae are theoretically free from histological inflamma-

tion but this "ideal" condition can only be established

experimentally in humans after supervised meticu-

lous daily plaque control for several weeks. Such fas-

tidious and time consuming oral hygiene measures

are uncommon and thus the gingivae we would rou-

tinely classify as "clinically healthy gingivae" are not

as histologically perfect as the "normal gingivae" de-

scribed. Clinically healthy gingivae would be typi-

cally that level of health which could be attained by

patients regularly practising a good standard of

plaque control.

Normal gingiva which is free from "significant"

accumulations of inflammatory cells may be better

described as "pristine gingiva". Thus, in the research

literature we have to deal with two types of healthy

gingivae, a super healthy or "pristine" state which

histologically has little or no inflammatory infiltrate,

and the "clinically healthy" gingiva which looks simi-

lar clinically but histologically features an inflamma-

tory infiltrate, and is the healthy gingiva we would see

clinically in everyday situations. The oral surface of "

clinically healthy gingivae" consists of keratinized

oral epithelium that is continuous with the junctional

epithelium (Fig. 5-la) and is firmly attached to the

tooth surface by hemidesmosomes. Neutrophils and

macrophages can be seen in the junctional epithelium.

Supporting the oral and junctional epithelia is connec-

tive tissue containing prominent collagen fibers which

maintain the form of the tissues in health and assist

the relatively weak hemidesmosomal attachment of

the junctional epithelium to the tooth. Below the junc-

tional epithelium is a vascular network which sup-

plies the epithelium with various nutrients and de-

fense cells and molecules (Fig. 5-1d).

The clinically healthy gingiva features an infiltrate

of inflammatory cells, predominantly neutrophils as-

sociated with the junctional epithelium and lympho-

cytes in the subjacent connective tissue (Page &

Schroeder 1976). Even in this very early stage of in-

flammation, which is not clinically detectable, colla-

gen depletion within the infiltrated area is noted along

with an increase in vascular structures. Exudative and