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Periodontology 2000, Vol. 38, 2005, 135–187 Copyright Blackwell Munksgaard 2005
Printed in the UK. All rights reserved PERIODONTOLOGY2000
Periodontal microbial ecology
SIGMUND S. SOCRANSKY &ANNE D. HAFFAJEE
The authors have taken the liberty of presenting this Periodontology 2000 will be to define the assemblage
manuscript in two parts. The first is a brief primer of species in the periodontal habitat, to determine
on microbial ecology, because, although the import- howchangesinthehabitataffectthecommunityand
ance of microbial ecology in periodontal diseases is howthe community affects its habitat.
widely recognized, most of us do not know precisely
what is meant by the term. The second section is a Habitat and niches
rather extensive overview of current studies of oral
microbial ecology based almost entirely on recent The habitat is the site at which a population or
in vivo studies. communitygrows,reproducesorsurvives.Theroleof
an organism in a habitat is its niche. Niche does not
connote location but rather function. A species can
Principles of microbial ecology haveonenicheinonehabitatandadifferentnichein
another habitat.
Microbial ecology is concerned with the interrela-
tionships between microorganisms and their envi- Microbial succession
ronments. Habitat ecologists, including periodontal
microbiologists, examine the microorganisms of a In a developing ecosystem, certain species termed
particular habitat and attempt to analyze the effects pioneer organisms colonize first. These species are
of the microorganisms on their environment and the often replaced by other species after they have
influence of the habitat on its residents. Many of the altered the habitat, making it suitable for colonization
principles of microbial ecology were outlined in a by other species. There are two kinds of microbial
superb monograph by Alexander (2) and will be succession. In autogenic succession, the sequence of
briefly described below along with some periodon- species is brought about because the resident popu-
tally relevant examples to highlight some of the lations alter their surroundings in such a manner that
points. they are replaced by species better suited to the
modified habitat. In allogenic succession, one type
The ecosystem of community is replaced by another because the
habitat is altered by nonmicrobial factors such as
Akey concept in microbial ecology is the ecosystem. changes in the physical or chemical properties of the
An ecosystem is the complex of organisms in a spe- region or changes in the host. Factors contributing to
cified environment and the nonmicrobial surround- succession are:
ings with which the organisms are associated. The • provision by one community of a nutrient that
ecosystem includes the assemblage of species and confers an ecologic advantage to the species in
the organic and inorganic constituents characterizing the next stage of succession;
that particular site. Each ecosystem has a collection • the making available by one population of a
of organisms and nonmicrobial components unique constituent present in insufficient supply to allow
to it and it alone. The organisms inhabiting a given for growth of a later population;
site constitute a community. The assemblage of • alteration in concentration of an inorganic nutri-
organisms constituting a community contains pop- ent;
ulations of individual microbial species. This leads to • modification of heterogeneous substrates such as
a hierarchy from ecosystem to community to popu- animal tissue;
lationtothesinglecell.Oneofthegoalsofthisissueof • an autointoxication effect;
135
Socransky & Haffajee
• elimination of an organism by physical means; that a change in habitat such as the development of
• the appearance of barriers due to environmental gingivitis also affects plaque development. Plaque
feedback. accumulated much more rapidly after cleaning, at
Thedevelopmentofgingivitis provides an example sites that exhibited gingivitis than at sites that were
of microbial succession as well as species habitat periodontally healthy (25, 132). Thus, it is possible to
interaction. Loe et al. (90) and Theilade et al. (170) postulate a scheme of microbial succession followed
demonstrated that dental plaque caused gingivitis. It by reciprocal host–bacterial interaction (Fig. 1). The
was shown that withdrawal of toothbrushing for membersofeachcolor-coded complex are described
28 daysinperiodontallyhealthyvolunteersresultedin in a later section. Initial colonization appears to
the rapid accumulation of plaque on the teeth. involve members of the yellow, green, and purple
Gingivitis developed in all subjects in 10–21 days. complexesalongwithActinomycesspecies.Thisleads
Re-establishmentoforalhygieneproceduresremoved to autogenic succession in which members of the
the plaque and reversed the gingivitis. Stained smear orange and then red complexes become more
preparations obtained during the 28-day time course dominant.Thepresenceofincreasedlevelsofthelast
revealed initial colonization by gram-positive cocci twocomplexes is hypothesized to lead to a change in
and rods, followed by gram-negative cocci and rods, the habitat, manifested clinically as gingivitis. The
then fusobacteria and filaments, and finally spirilla gingivitis in turn favors further proliferation by
and spirochetes. Appearance of clinical gingivitis members of not only the orange and red complexes,
related to the appearance of the gram-negative forms. but probably membersoftheearlycolonizing species
These data were in accord with other studies that as well. This cycle could be broken in a number of
demonstrated microbial succession in plaque devel- ways. The first way would be to eliminate all plaque;
opment(140, 161,188).TheDanishstudiesassociated this partially successful strategy is the one most
certain bacterial morphotypes with a change in the commonly employed today. The second would be to
clinical status of the site, i.e. the development of eliminate members of the red and⁄or orange
gingivitis. Data presented below demonstrate that complexes.Thiswouldprobablylimitgingivitisandits
species of the red and orange complexes (described feedback effect of greater plaque development. The
later)aremoreprevalentandfoundinhighernumbers third would be to decrease gingivitis by a non anti-
in lesions of established gingivitis. The same taxa are microbial approach, leading to decreased plaque
even more prevalent and found in higher numbers in accumulation and possibly diminished red and
suppurating lesions. Thus, a change in plaque orange complex development. It is worth noting that
compositionappearstoaffectthehabitat,resultingin theeffect of a prevention or treatment regimen would
clinically apparent gingivitis. Other studies indicate be an example of allogenic succession.
Microbial succession Reciprocal interaction
Purple
Actinomyces sp.
Yellow Orange Red Gingivitiis
Green
Fig. 1. Hypothesized relationship between the addition of inflammation would result in increased growth of
species during microbial succession leading to the devel- colonizing species.
opment of gingival inflammation. In turn, the increased
136
Periodontal microbial ecology
Factors limiting colonization from subject to subject. Microorganisms show cen-
ters of dispersal, regions from which species are
Certain factors limit colonization. One obvious limi- spreading or have spread. At this site, conditions are
tation is the available physical space. Preemptive favorable for an increase in density of the species and
colonization is a second situation in which prior the site serves as a point from which the species can
colonization by one species excludes another. emanate. This site is referred to as a reservoir of
Exclusion results from the occupation of a niche by infection. The greater the efficiency of the dispersal
one species that might have been taken by the other. mechanism, the smaller the number of organisms
The first species performs the activities, uses the needed for dispersion. Oral species might dissemin-
nutrients and⁄or occupies the physical sites of ate from subject to subject via droplet infection or
the excluded species. Environmental resistance is the infection via inanimate objects. The tools of
restriction in numbers of individuals or biomass molecular epidemiology have been used to demon-
imposedbyphysical,chemicalorbiologicalfactorsof strate vertical transmission (parent to offspring) for
the ecosystem. The condition holding the population Actinobacillus actinomycetemcomitans (124, 125, 128)
in check is considered to be a barrier. Preemptive and Porphyromonas gingivalis (125), as well as hori-
colonization is a major means of exclusion of late- zontal transmission from spouse to spouse for
comers, and it is, together with the physical and P. gingivalis (143, 175). Another example of trans-
chemical barriers in the locale, one of the compo- mission comes from early studies of acute necrotiz-
nents of environmental resistance. Any periodontal ing ulcerative gingivitis, also known as Trench
investigator who has attempted to introduce a test mouth.Thisdiseasewastransmittedamongtroopsin
species into periodontal plaque can attest to the WorldWarIandlatertothecivilianpopulation(154).
effectiveness of these barriers. Riviere et al. (141) found that spirochetes and
P. gingivalis were more prevalent in diseased sites of
Dissemination of organisms diseased subjects than in healthy sites of diseased
subjects (Fig. 2). Of major significance was the
In order for organisms that are restricted in nature to additional finding that healthy sites of diseased sub-
live in association with a suitable host to continue to jects harbored these species more frequently than
survive, their dispersal is essential. Dissemination healthy sites of healthy subjects. This finding has
can be via active or passive means. For example, been confirmed in other studies, as will be described
growth or motility can actively move a species from below. The authors speculated that the deeper
one site to another within the oral cavity. Passive pockets of diseased subjects were acting as reservoirs
dissemination occurs both within the oral cavity and for spread of infection to healthy sites. This is indeed
Spirochetes 16 P. gingivalis
60 154
% sites Health 342
Gingivitis 136 154
45 Early periodontitis 12
1214 360
Advanced periodontitis 408 363
342 8
30 363 609
360
1214 609
15 4 1708
136 1708 268
268 408
0 0
Health Gingivitis Early Advanced Health Gingivitis Early Advanced
Periodontitis Periodontitis Periodontitis Periodontitis
51161 29 5 11 61 29
Fig. 2. Bar charts of the frequency of detection of spiro- number of samples examined. The bar colors indicate
chetesandP. gingivalisinsitesandsubjectswithdifferent the characteristics of the sampled site. The labels under
clinical characteristics. Spirochetes were identified using the bars indicate the classification of the subject, and the
phase contrast microscopy and P. gingivalis by immuno- numbers under the bars indicate the number of subjects
cytochemistry. The numbers over the bars indicate the examined. Data adapted from (141).
137
Socransky & Haffajee
a possibility, although alternative hypotheses are The climax community
possible.
The interaction between the microbial and nonmi-
Infectious disease crobial components of an ecosystem ultimately leads
to a form of stabilization in which microbial and
Infectious diseases represent a category of popula- nonmicrobial forms exist in harmony and equilib-
tion–environment interactions involving a host plus a rium with their environment. This is the climax
microorganism with the potential for both coloniza- community. This remains reasonably stable over
tion and pathogenesis. From the ecologic standpoint time and reflects a dynamic situation in which cells
the governing feature of the ecosystem is the living are dying and being replaced. The climax is essen-
animal⁄human. The host must be colonizable, i.e. it tially a self-replicating entity that reproduces itself
must be receptive to invasion by the particular dis- with remarkable fidelity. Given the same initial
ease agent. Not all higher animals are colonizable by physical and chemical site characteristics or identical
all pathogenic bacteria, fungi or viruses. Three kinds hosts, the same general successional sequences will
of barriers underlie lack of receptiveness: be initiated and fostered, giving rise to remarkably
• the barriers of the nonreceptive host; similar climax communities. The climax can be
• the factors associated with the resistance of the modifiedfromtimetotimebyexogenousforces.The
receptive host prior to its first contact; equilibrium tends to be restored as the habitat
• the obstacles to further bacterial development or returns to its original state. At other times, environ-
activity that appear as a consequence of infection. ments may be irreversibly altered, leading to a dif-
In effect, there is an environmental feedback, a ferent steady state and a different climax community.
modification of the habitat resulting from the pres- The climax contains many niches and the species
ence of one or more bacterial populations, a change occupyingeachisuniquelyfit,atleastamongspecies
that can affect the size, activity or survival of the having access to the locale, for the function associ-
invading population or one or more segments of the ated with the niche. Inasmuch as there are numerous
community. The production of antibody to colon- niches or potential functions, particularly when there
izing species is an example of environmental feed- is an intermeshing of food chains, many physiologi-
back. This will be discussed in greater detail later in cally different groups of organisms can coexist
this chapter. indefinitely.
Most developed dental plaques represent climax
Successful colonization communities. Minor perturbations probably result in
are-developmentofthesamecommunity,albeitwith
Success in colonization of a species depends on somewhat altered proportions of species. Preventa-
• presence at the colonizable place at the correct tive or therapeutic strategies probably encounter a
time; tendency of the ecosystem to return to the original
• possession of survival capability permitting pro- equilibrium after termination of treatment. This
longed viability in deleterious circumstances; tendency can be frustrating to the clinician in that it
• ability to obtain all nutrients from the ecosystem; necessitates a prolonged maintenance phase after
• capacity to tolerate all of the ecologically signifi- therapy. Often, we wish for more profound changes
cantnonmicrobialfactorsoftheenvironment,e.g. in the periodontal microbiota after therapy. However,
pH, O2 levels, temperature, osmotic pressure, as the old adage states: be careful what you wish for,
oxidation reduction potential; because you might get it. More permanent changes
• possession of mechanisms to overcome or cope canbebroughtaboutinthemicrobiotabyemploying
with environmental resistance attributable to potent exogenous forces of a persistent nature. The
viable hosts; microbiota of a recent refractory patient is instruct-
• ability to overcome or cope with environmental ive. The subject is a dental professional who exhib-
resistance attributable to species already in the ited initial signs of periodontitis about 10 years ago.
habitat; Hewastreatedinitiallybyscalingandrootplaningand
• capability to grow as rapidly as one’s neighbors; later by surgery. The disease continued to progress,
• ability to adhere to appropriate surfaces. leadingtothelossoffiveteethin2 yearsaccompanied
The role of some of these factors in the formation of by a very painful symptomatology. He took in
microbial complexes was discussed in Socransky sequence: systemic tetracycline, ampicillin, amoxicil-
et al. (156). lin + metronidazole,clindamycin,ciprofloxacin,long-
138
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