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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 ...

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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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...Periodontology vol copyright blackwell munksgaard printed in the uk all rights reserved periodontal microbial ecology sigmund s socransky anne d haffajee authors have taken liberty of presenting this will be to dene assemblage manuscript two parts rst is a brief primer species habitat determine on because although import howchangesinthehabitataffectthecommunityand ance diseases howthe community affects its widely recognized most us do not know precisely what meant by term second section and niches rather extensive overview current studies oral based almost entirely recent site at which population or vivo communitygrows reproducesorsurvives theroleof an organism niche does connote location but function can principles haveonenicheinonehabitatandadifferentnichein another concerned with interrela tionships between microorganisms their envi succession ronments ecologists including microbiologists examine developing ecosystem certain termed particular attempt analyze effects pioneer organism...

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