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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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