牙周微生物学
葛少华
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Email: shaohuage@sdu.edu.cn
Tel: 88382123
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主要内容
Microecosystem of periodontium
Pathogenicity of microorganism
Microorganism of periodontal disease
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第一章 牙周微生态系
Microecosystem of periodontium

概念：正常菌群之间及其与宿主之间的相互作用
称为微生态系（microecosystem）
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一、牙周微环境的特性
从微生态角度来看，口腔是一个复杂完整的
生态区，由众多生态系(niche)组成，每个生
态系的微生物都可能与口腔的健康和疾病有关。
牙周作为一个相对独立的微生态系，具有自己
的特性。
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牙龈、牙周膜、牙槽骨和牙骨质这些牙周组织的解
剖结构和理化特性各不相同。牙周病独特受犯部位
的解剖结构表明，身体其他部位在软硬组织之间没
有如此复杂的关系，形成有氧到无氧各种不同氧张
力环境和许多特殊的微环境。
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一、牙周微环境的特性
它们又处于唾液和龈沟液的包围之中，牙周局
部有适于微生物生长的温度、湿度和营养，给
许多微生物的生长、繁殖和定居提供了适宜的
环境和条件。
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牙周菌丛的特点：
①种类多：500多种，有需氧菌，兼性厌氧菌和厌
氧菌及真菌，支原体，螺旋体和病毒。
②细菌数量大：唾液中的细菌为108/毫升，而牙
菌斑中的细菌更多，约为5×1011/克湿重
③细菌的寄生期长，终生伴随宿主，从出生3-4h
直至死亡。
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牙周正常菌群之间的关系

共生（symbiosis）

竞争（competition）

拮抗（antagonism）
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英国科学家A.Fleming爵士
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影响牙周生态系的因素
牙周组织的解剖结构及理化特性
口腔微生物在牙周的定居，主要取决于不同牙
周组织的解剖结构的改变及表层细胞的特性。
 唾液的量、成分、流速及龈沟液的作用
 牙周微环境（microenvironment）的组成
 微生物之间的相互作用：symbiosis,competition,
antagonism

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牙周微环境的组成
1 营养源
2 氧化还原电势（Eh）
3 pH
4 温度
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牙周微环境的组成-营养源
营养源：细菌生长繁殖需要营养，牙周微生物生
长繁殖所需要的营养物主要来自宿主摄入的食物。
Unlike dental caries, many of the bacteria associated
with periodontal diseases are asaccharolytic(i.e. cann
ot metabolize carbohydrates for energy) but are prete
olytic.
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牙周微环境的组成-Eh
牙周生态各部位，可因氧化型物质和还原
型物质的比例不同，而使Eh有明显差异。
如氧化型物质浓度高于还原型物时，Eh为
正值，反之为负值。
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Eh
一般唾液和黏膜表面的Eh较高
部位
Eh
唾液
+240～+350mv
黏膜表面
+60～+120mv
正常龈沟
+75～+100mv
随牙周袋的加深，Eh逐渐下降，可从
+100mv降至-300mv
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Eh
不同细菌对氧的敏感程度不同
细菌
Eh
需氧菌
+300mv
厌氧菌
+100～-200mv
兼性菌
高于+100mv 有氧呼吸
低于+100mv 无氧酵解
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牙周微环境的组成-pH
pH:5.0～8.0 但在口腔某个微环境中可出现较大幅
度的改变，影响微生物种类和数量。
Just mentioned as formerly, a consequence of proteolysis
is that the pH in the pocket during periodontal disease be
comes slightly alkaline(Ph7.4-7.8)compared to near neutral
values in health(pH6.9).Moreover, the growth and enzyme
activity of periodontal pathogens such as Pg is enhanced by
alkaline growth conditions.
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牙周微环境的组成-温度
温度：病原菌的生长适宜温度近体温。
The temperature of the periodontal pocket can
increase slightly during inflammation.
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Therefore, the change in local enviroment(e.g.
the increase flow of GCF that occurs during the
inflammation , and the resulant increase in pH
and tempertature) favor the growth of the proteolytic
and obligately anaerobic species(many of which
are Gram negative). This results in a shift in
the overall balance of the subgingival microflora,
thereby predisposing a site to disease.
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二、牙菌斑（dental plaque）
1、牙菌斑的概念及作用
牙菌斑是一种寄居在牙齿表面的以细菌为主体的生态环境，
是细菌在牙面上生存、代谢、致病的具体环境，它有形态、
有结构、有代谢活动，是龋病和牙周病的主要病因。
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牙菌斑既是龋病的病因，又是牙周病的病因，但
引起龋病和牙周病的菌斑的性质不同，它们作用
的组织和所处的环境也不同。
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致龋菌斑和致牙周病菌斑区别
致龋菌斑
病原菌
致病物质
致病机制
变链和乳杆
乳酸
牙脱矿
龋病
致牙周病菌斑
厌氧菌（Pg,Aa,Pi,Bf）
toxin,enzyme,etc.
损害牙周组织
牙周病
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2、牙菌斑的形成
牙菌斑形成的三个阶段：
获得性薄膜的形成
细菌黏附与共聚
菌斑成熟
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Acquired Pellicle
A thin film (about 1 um), derived mainly from sali
vary glycoproteins, which forms over the surface
of a cleansed tooth crown when it is exposed to t
he saliva.
 Synonym: acquired cuticle, acquired enamel cuti
cle, brown pellicle, posteruption cuticle.

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Pellicle Formation:
The first stage is the formation of an organic dental
pellicle, also known as the acquired or salivary pellicle.
It is an amorphous, tenacious, membranous film, about
1-2 microns thick, that forms on teeth and other solid
intra-oral surfaces (restorations; calculus; orthodontic
appliances, dentures,etc.)
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It is easily removed by brushing but begins reforming in
minutes and completely reforms very quickly.
Bacteria are not required for pellicle formation, but
they adhere to and colonize it shortly after the pellicle
is formed.
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Bacterial Colonization:
Bacteria borne in the saliva are continually being
brought into contact with the organic dental pellicle.
Some bacteria are retained in surface irregularities such
as pits, fissures or open restorative margins. Others
actively adhere to the pellicle by interacting with it.
This interaction is determined by specific surface
characteristics found on bacterial cell surfaces
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Oral bacteria vary significantly in their ability to intera
ct with the pellicle due to variations in their cell surface
coatings. A group of protein molecules called adhesions
located on the bacterial cell surfaces recognize and link
to the pellicle glycoproteins promoting attachment of
specific bacteria with the initial colonization of the
pellicle, plaque is formed.
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Growth and Maturation of Plaque
Plaque, once disturbed, takes approximately
twenty four hours to reform. This initially form
ed plaque is known as immature plaque. Immat
ure plaque is generally lighter in color, less adhe
rent and less potentially pathogenic. As plaque
matures it increases in mass and thickness. Its
microbiologic composition also changes. Mature
plaque is potentially more pathogenic.
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Plaque Retention Factors
These are conditions that favor plaque
accumulation and hinder plaque removal by
the patient and the dental professional.
Examples of these are:
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








Orthodontic Appliances
Partial Dentures
Malocclusions
Faulty Restorations
Calculus
Deep Pockets
Mouth Breathing
Tobacco Use
Certain Medications
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
Orthodontic Appliances
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
Partial Dentures
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•Malocclusions
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•Tobacco Use
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It is important that the patient be adequately educated
in the cause and progression of periodontal diseases.
Patients need to understand the importance of brushing
and flossing and the need to remove plaque and calculus
to maintain the health of their teeth and gums.
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Disclosing agents can be a very useful tool in
showing patients where the plaque is and how
it can be effectively removed. The educational
aspect is as important as the technical skills and
this must be communicated to the patient.
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Plaque along the interproximal and gingival margin,
stained pink-red by discolosing solution
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3、牙菌斑的结构
电镜下
分三层
基底层：无细胞的均质结构
获得性膜+上皮剩余
中间层：菌斑的主要组成部分
丝状菌+杆菌
栅栏结构
外层：细胞排列紊乱，松散
球菌+短杆菌
玉米穗样
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4、牙菌斑的分类
supragingival plaque
Dental plaque subgingival
attached
plaque
unattached
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Supragingival plaque is bacteria adher
ent above the gingiva, whereas bacteria
below the gingiva is called subgingival
plaque.
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Growth in supragingival plaque mass
results from nutrients obtained from
ingested simple carbohydrates
(glucose), lactic acid and other plaque
components.
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Subgingival (plaque) bacteria preferentially uses
metabolized peptides and amino acids over glucose th
at are obtained from tissue breakdown products, th
e gingival crevicular fluid. Inflammed gingival
tissues produce more gingival crevicular fluid which
favors the proliferation of subgingival bacterial
replication.
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Subgingival bacterial populations prefer a no oxygen
(anaerobic) environment, whereas supragingival
bacterial populations prefer a low oxygen environment,
and are called facultative anaerobes. Long-standing
plaque is mostly composed of gram-negative anaerobes.
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The persistence of microbial plaque can
lead to the development of caries, gingivitis,
calculus formation, gingival recession, and
various manifestations and types of
periodontitis.
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Supragingival plaque
窝沟菌斑
龈上菌斑 光滑面菌斑 与龋病有关
龈缘菌斑
与龈炎有关
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龈上菌斑的组成及致病性
龈上菌斑由增殖的微生物+上皮细胞+PMN+巨噬细
胞组成。成人龈上菌斑中最常见的细菌为轻链球
菌、表皮葡菌、粘放菌、奈氏放线菌，主要为革
兰氏阳性的需氧菌和兼性菌。在龈炎发展的后期，
会有较多的革兰氏阴性菌出现。龈上菌斑与龋病
龈炎的发生、龈上牙石的形成有关。
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龈上菌斑
龈上菌斑还为龈下菌斑的形成提供了附着部位、
生长所需的营养和低的Eh等。经常的清除龈上菌
斑有助于防止龈下菌斑的形成。
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龈下菌斑
龈缘以下牙周的软性未钙化的细菌沉积物
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1、龈下菌斑的分类
大多数学者将龈下菌斑分为两部分，即attache
d and unattached ,Newman and Saglie（1984）对龈下
菌斑进行了更为详细的描述：
1、tooth-associated subgingival plaque, also called attached
subgingival plaque, densely organized
2、tissue-associated subgingival plaque, unattached subgingi
val plaque, loosely organized
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附着性龈下菌斑
附着在龈沟和牙周袋内相应的牙面上。以革兰氏
阳性杆菌和球菌占优势,如轻链、血链、优杆菌、
粘放、内放、丙酸杆菌、马氏丝杆菌等，此外还
有一些革兰氏阴性的球菌和杆菌。此类菌斑不延
伸至结合上皮。附着性菌斑与龈下牙石的形成、
根面龋和根吸收有关。
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非附着性龈下菌斑
epithelium-associated subgingival plaque :是一种结构疏
松的菌斑团块，直接与龈下的上皮相关，从龈缘延伸到结
合上皮。在此区中一部分菌斑与上皮接触或黏附在上皮表
面；另一部分游离于袋内壁上皮和根面之间的腔隙内。已
有研究表明，牙周微生物特有的表面结构，如pilus, vesicl
e含adhesin,能选择性的黏附在龈沟或牙周袋内壁上皮的
受体上。
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非附着性龈下菌斑
由于与上皮相关的菌斑，可与龈沟或牙周袋内壁
上皮及袋底的结合上皮直接接触或黏附，有些微
生物可入侵上皮内或结缔组织中，甚可达骨面。
因此，临近龈沟和结合上皮的菌斑可能是牙周损
害的进展前沿（advancing front），毒力力强，
与牙槽骨的快速破坏有关。
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2、龈下菌斑的特点
不同类型的牙周炎或同一类型牙周不同的
时期（活跃期和静止期），龈下菌斑的菌
群组成各有不同。
与牙齿相关的附着性龈下菌斑菌群的组成，通常
认为是以革兰氏阳性细菌占优势；
与组织相关的龈下菌群则随病变的活跃期和静止
期发生改变。
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


在病变活跃期，以革兰氏阴性杆菌和螺旋体占优势。
在病变静止期或经牙周治疗后，则以革兰氏阳性和阴
性球菌占优势。
当牙周病变处于活跃期时，与上皮相关的龈下菌斑体
积增大，微生物的数量增加。相反，当病变处于静止
期时，此类菌斑的体积相对减小。微生物的数量也随
之改变。
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牙周菌斑微生物致病学说
The role of plaque bacteria in periodontal diseases:
 Non-specific
plaque hypothesis
 Specific plaque hypothesis
 Ecological plaque hypothesis
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Our understanding of the relationship between
the microorganisms found in dental plaque and
the common dental disease of periodontitis has
undergone numerous phases historically.
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Early in the 19th century, it was felt that, like the situation
with diseases such as tuberculosis, a specific bacterial species
was responsible for the disease processes. The criteria by
which a given bacterial species was associated with disease
historically has been through the application of Koch's
Postulates. These criteria were developed by Robert Koch in
the late 1800s. The criteria are as follows:
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



1. A specific organism can always be found in association
with a given disease.
2. The organism can be isolated and grown in pure culture
in the laboratory.
3. The pure culture will produce the disease when inoculated
into a susceptible animal.
4. It is possible to recover the organism in pure culture from
the experimentally infected animal.
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However, the concept that a specific bacterial
species was responsible for periodontal diseases fell
out of favor for several reasons.
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First, despite numerous attempts, a specific bacterial agent
was not isolated from diseased individuals. Rather, the
organisms found associated with disease were also found as
sociated with health. Good experimental animal model
systems of periodontal disease were not available to test the
pathogenicity of specific microorganisms (this, in fact,
remains problematic today).
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Further, in the mid 1900's, epidemiological studies indicated
that the older an individual was, the more likely they were
to have periodontal disease. This led to the concept that the
bacterial plaque itself, irrespective of the specific bacteria
found in plaque, was associated with disease. This concept,
known as the Non-Specific Plaque Hypothesis (Miller, 1890),
held that all bacteria were equally effective in causing
disease.
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非特异性菌斑假说
（1890 Miller）
内容：牙周病是由非特异性的口腔正常菌群混合
感染所致。该学说强调菌斑细菌的量，认为牙周
病的发生发展是菌斑内总体微生物联合效应的结
果。
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Disease onset and progression were thought to result
from the increase in plaque beyond a threshold level
at which the plaque bacteria and their toxic products.
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非特异性菌斑假说
（1890 miller）
依据：
①将健康者或牙周病患者的牙菌斑悬液接种于动
物皮下，均可引起脓肿。
②临床看到菌斑牙石多者，牙龈炎症较重。
③总体清除菌斑或减少菌斑量，对治疗牙周病有
效。
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Several important developments caused a change
in this thinking.
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Many individuals with considerable amounts of plaque,
calculus and gingivitis never develop destructive
periodontal diseases.
The pattern of disease evident in individuals with
periodontitis reveals advanced lesions adjacent to
sites that are largely unaffected.
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In addition, it was realized that organisms that are found as
part of the "normal" bacterial flora (i.e., found in health),
may function as pathogens under certain conditions. These
organisms may be altered, or increase significantly in
numbers relative to other non-pathogenic species, to
function as pathogens. This type of bacterial pathogen is
referred to as an endogenous pathogen, in contrast to an
organism that is not normally found in healthy states which
is termed an exogenous pathogen.
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Moreover , tremendous advances were made in
the 1960's and 1970's in techniques used to culture
anaerobic microorganisms (bacterial species that
cannot grow in the presence of oxygen). These
advances were related to the anaerobic culturing
conditions as well as the nutrients required in
media to grow anaerobic species, which are
typically very fastidious in their nutrient requirements.
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The growth of anaerobic microorganisms, and examination of
their properties using in vitro and in vivo model systems, has now
led us back to the understanding that different microorganisms
have varying potential to cause disease. Thus, the current concept
of the processes involved in the development of periodontal
diseases fall under the Specific Plaque Hypothesis (Loesche,1976)
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The Specific Plaque Hypothesis states that disease
results from the action of one or several specific
pathogenic species and is often associated with a
relative increase in the numbers of these organism
found in plaque.
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An underlying tenet of the specific plaque hypothesis
is that bacteria are not equally pathogenic, and thus
specific bacteria in plaque are responsible for the
changes that lead to destructive periodontitis.
Acceptance of the specific plaque hypothesis was
furthered by the recognization of Aa as the
predominant pathogen in LAgP.
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特异性菌斑假说
（1976 Loeche）
内容：牙周病可能是一组病因和进程各异而临床症状相似
的疾病，即认为不同类型的牙周病是由不同的特异性细菌
所致。该学说强调细菌的质，认为菌斑不是均质的细菌团
块，在牙周健康区和病损区、不同类型的牙周病损区之间，
菌斑微生物的构成不同，在为数众多的口腔微生物中，绝
大多数细菌是口腔固有菌丛，只有少数具毒力和损害宿主
防御机能的特殊致病菌，才对牙周病的发生发展起关键作
用。
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特异性菌斑假说
（1976 Loeche）
依据：①流行病学调查发现，健康人与牙周病患者的菌斑微
生物组成不同，不同类型的牙周炎各有自己的优势菌。
②牙周病动物实验模型的研究发现，将从LAgP分离出的
Aa, Cap no .gingivalis,从CP中分离出的Pg,Bf 接种在悉生
大鼠口腔中能引起牙槽骨吸收；而从健康人或牙龈炎的菌
斑中分离出的一些细菌则不引起大鼠的牙槽骨吸收。
③在临床治疗中，有些病例称为“难治性牙周炎”，即使进
行反复的菌斑控制，包括牙周手术，仍不能阻止病变的发
展。只有消除某些特异的微生物才有可能获得成功。
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A form of Koch's Postulates specifically oriented
to the situation in periodontal diseases has been
proposed by a microbiologist by the name of
Socransky (Socransky & Haffajee, 1992).
Socransky's criteria for periodontal pathogens are
as follows:
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ASSOCIATION: A pathogen should be found
more frequently and in higher numbers in disease
states than in healthy states
2. ELIMINATION: Elimination of the pathogen
should be accompanied by elimination or remission
of the disease.
3. HOST RESPONSE: There should be evidence of a h
ost response to a specific pathogen which is
causing tissue damage.
1.
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4. VIRULENCE FACTORS: Properties of a putative
pathogen that may function to damage the host
tissues should be demonstrated.
5. ANIMAL STUDIES: The ability of a putative
pathogen to function in producing disease should be
demonstrated in an animal model system
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The two periodontal pathogens that have most
thoroughly fulfilled Socransky's criteria are Actino
bacillus actinomycetemcomitans in the form of
periodontal disease known as LAgP, and Porphyro
monas gingivalis in the form of periodontal disease
known as CP. Selected properties of these microorganisms that have been associated with disease
are summarized in the following tables.
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Evidence implicating Porphyromonas gingivalis
as a periodontal pathogen
(Adapted from Socransky, 1992)
CRITERION
Association
Elimination
OBSERVATIONS
Microorganism is elevated in periodontitis lesions
Unusual in health or gingivitis
Suppression or elimination results in clinical resolution
Elevated systemic and local antibody in periodontitis
Collagenase, trypsin-like enzyme, fibrinolysin,
Virulence Factors
immunoglobulin degrading enzymes, other proteases,
phospholipase A, phosphatases, endotoxin, hydrogen
sulfate, ammonia, fatty acids and other factors that
compromise PMN function
Animal Studies
Onset of disease correlated with colonization in
monkey model
Key role in mixed infections in animal models
Host Response
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牙周病与牙周微生态失调
1、normal flora ：正常菌群是在长期的历史进化过
程中，微生物通过适应和自然选择的结果。在牙
周微生态系中，微生物与微生物之间、微生物与
宿主，以及微生物和宿主与外界环境之间呈动态
平衡状态，形成一个相互依存、相互制约的统一
体。
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牙周病与牙周微生态失调
2、normal flora的作用：正常微生物群在宿主体内构
成一个重要的对抗外来病原微生物侵袭和定植的保
护屏障，即定植抗力（colonization resistence）。
宿主的健康、营养和局部外环境的改变等诸多因素
都能影响微生物群的稳定性。当其稳定性破坏时，
导致正常微生物的比例失调或潜在的病原微生物定
植，从而引起感染和疾病。
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牙周病与牙周微生态失调
Small amounts of plaque can be controlled
or tolerated without causing periodontal
disease
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When specific bacteria within the plaque either
 increase to sufficient numbers
 produce virulence factors
 both
the balance shifts towards disease production
Disease can also occur by a reduction in the hos
t defense capacity (AIDS)
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3、牙周微生态失衡（dysbiosis）:从微生态观点出
发，牙周微生态失衡是牙周病发生发展的关键。
当宿主抵抗力下降或牙周局部环境改变时，菌斑
内的微生物，特别是那些不利于牙周组织健康的
微生物过度生长繁殖，在数量上偏离了正常的生
理组合，菌斑中原有的微生物之间动态平衡的稳
定性遭到破坏，在此种状态下有利于外来的病原
微生物侵袭牙周或口腔其他部位。
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Ecological plaque hypothesis
Based on the influence of enviromental parameters
on the ecology of plaque biofilms, the ecological
plaque hypothesis has been proposed as an
alternative to the Specific plaque hypothesis.
It maintains that the microbiota undergoes a transition
from a commensal to a pathogenic relationship with
the host due to factors that trigger a shift in the
proportions of resident microorganisms.
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Ecological studies based on the detection of 40
different species in over 13,000 plaque samples
have defined five major bacterial “complexes”,
each consisiting of bacterial species that are found
in associated with one another in the plaque enviroment.
The potential for pathogenicity is highest in the red
group and lowest in the yellow group.
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The “red complexes”,which includes P.gingivalis,
Tannerella forsythia(Bacteroides forsythus) ,and
Treponema denticola, were found to be associated
with increased pocket depth and BOP.
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牙周病与牙周微生态失调
潜在性病原微生物在牙周的定植，也有可能使
原本寄居在牙周的属于亚临床感染的外源病原
微生物生长繁殖，使菌斑性质发生从量到质的
根本变化，从而表现出明显的致病性，导致牙
周支持组织的破坏。
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牙周生态调整
牙周病的防治方面，采取保持和调整其微生态平衡的措施：
 利用牙周正常菌群在生态学上的稳定性和优势阻止外源性
致病菌的定植；
 研究牙周菌群各种复杂的共生和拮抗关系，并从中找出规
律，扶植那些有利于牙周健康的细菌，使之保持优势去抑
制那些对牙周健康有害的细菌（生物替代疗法）。
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牙周生态平衡、失衡及调整
细菌
侵袭力包括：
细菌种类数量定位
内毒素酶毒性产物
牙周组织
侵袭力＝防御力
生态平衡（动态）
牙周健康
侵袭力增强：
细菌种数定变化
牙石食物嵌塞
口呼吸咬和创伤
侵袭力＞防御力
生态失调
侵袭力降低：
去除菌斑
合理应用抗菌药物
建立拮抗菌丛
侵袭力＜防御力
生态调整
牙周病
宿主
防御机能包括 ：
上皮屏障、炎症细胞
免疫反应、组织修复
防御力下降：
内分泌F（DM）
营养F（VitC缺乏）
遗传F（DOWN）
防御力增强：
调整宿主防御能力
补充营养，增强体质
牙周病防治
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back
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Chapter 2 Pathogenic Mechanisms
in Periodontal Diseases
The organisms may produce the diseases


indirectly
direct invasion of the tissues
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Potential Bacterial Mechanisms in Period
ontal diseases
Bacterial invasion of tissues
Exotoxins
Cell constituents (such as endotoxins)
Histotoxic end products
Enzymes
Immunologic -host responses
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Bacterial Invasion of Tissues

Originally it was thought that bacteria didn’t
actively invade the periodontium

They were thought to act only through enzym
es or toxins or through an antibody response
to their antigens
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

More recently, it’s been shown that bacteria
can invade the periodontal tissues
Some of the bacteria that have been identified
are shown in the next table
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Presence of Bacteria in Tissues
Chronic Periodontitis:
 Porphyromonas gingivalis
 Prevotella intermedia
 Capnocytophaga sputigena
 Capnocytophaga gingivalis
Aggressive Periodontitis:
 Actinobacillus actinomycetemcomitans
ANUG (NUP):
 Prevotella intermedia
back
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Exotoxins
Many bacteria produce exotoxins (Corynebacterium
diphtheria, Streptococcus pyogenes, Clostridium bo
tulinum)
Generally, the recognized periodontopathogens are
not known to produce toxins
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An exception is the leukotoxin of A. actino
mycetemcomitans
This leukotoxin may enable A. a to destroy
leukocytes in the gingival crevice, assisting
the microorganism in its ability to colonize
and invade the gingival tissues
back
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Cell Constituents
Cellular constituents of Gram-positive and Gramnegative bacteria may also play a role in
periodontal disease
These include :
endotoxins
Gram-negative bacteria
bacterial surface components Gm+
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Large numbers of Gram-negative bacteria
in pockets = high concentrations of
endotoxin
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Activities of Endotoxin
Produce leukopenia
 Activate the clotting system
 Activate the complement system by the alternate
pathway
 Lead to a localized Schwartzman phenomenon wit
h tissue necrosis following multiple exposures to
endotoxin
 Induce bone resorption in organ culture
 Produce cytotoxic effects on cells such as
fibroblasts
 Activate macrophages to synthesize cytokines

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Activities of Peptidoglycan
Peptidoglycan (in cell walls of Gram-positive
bacteria) affects the host in many ways as
shown in the next table
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Complement activation
 Immunosuppressive activity
 Stimulation of the reticuloendothelial system
 Bone resorption
 Stimulate macrophages to produce prostagla
ndin and collagenase

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PGE2
may play a central role in the tissue
destruction that occurs in periodontal diseases.
Levels of PGE2 in periodontal tissue are low or
undetectable in health, increase in gingivitis, and
rise significantly in periodontitis. Now there is
increasing evidence that the level of PGE2
produced in response to bacterial challenge
(especially by endotoxin) can be used as a
measure of susceptibility (Offenbacher et al. 1993).
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Presumably,
the level of PGE2 production
is subject to genetic influence. Studies of
identical and fraternal twins, either reared
together or apart, provide evidence that
genetic factors may indeed influence
susceptibility or resistance to the common
adult form of periodontitis (Michalowicz
1994).
back
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Histotoxic Bacterial End Products
Both Gram-positive and Gram-negative
subgingival bacteria produce a wide
variety of toxic end products that are capable
of tissue destruction
These are shown in the next table
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





Fatty acids
Organic acids such as butyric（丁酸） and propionic
acids（丙酸）
Amines（胺）
Volatile sulfur compounds
Indole
Ammonia（氨）
back
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Enzymes
Many of the bacteria in the pocket are able to
produce enzymes that may play a role in peri
odontal disease initiation and progression
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1.Hyaluronidase
Hyaluronidase influences gingival permeability
occurs in higher concentrations in periodontal
pockets than in healthy sulci
There are more hyaluronidase producing bacteria
in the periodontal pockets than supragingivally
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Topical application of hyaluronidase to gingival
epithelium leads to widening of the intercellular
spaces and increased permeability
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2.Collagenase
Collagen is degraded in periodontal disease
Mainly due to tissue collagenase but also
due to bacterial collagenase Porphyromonas
gingivalis and some strains of A. actinomyce
temcomitans produce collagenase
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3.Gingipain
Porphyromonas gingivalis produces many
proteinases
Some are called as “gingipains” (derived from
the words gingivalis and papain a proteolytic
enzyme)
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

Three of these gingipains (HRGP, RGP2, KGP)
rapidly degrade TNF-alpha, a proinflammatory
cytokine
This cytokine is important to the function of p
olymorphonuclear leukocytes and it can suppr
ess viral replication and activate phagocytes
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These and other bacterial enzymes of
suspected periodontopathogens that
may cause periodontal destruction
include those shown in the next table
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Bacterial Enzymes That May Cause Period
ontal Destruction
Elastase
Collagenase
Gelatinase
Aminopeptidases
Phospholipase A
Alkaline phosphatase
Acid phosphatase
Hemolysin
Keratinase
Arylsulfatase
Neuraminidase
DNAse
RNAse
back
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Immunologic-Host Responses
Bacterial factors also aid in evasion of host
defenses as shown in the next table
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Bacterial Factors Important in Evading
Host Defenses
Inhibition of PMNs：
Leukotoxin ：killer -PMN
Chemotaxis inhibitors
Decreased phagocytosis and intracellular killing
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Chemotaxis
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Once a white cell has left the blood vessel and migrated to the enemy, the
next job is to EAT the microbe. This human macrophage, like its cousin
the neutrophil, is a professional "phagocyte" or eating cell (phago =
"eating", cyte = "cell"). The macrophage is using its internal cytoskeleton
to envelop cells of the fungus Candida albicans.
But eating the organisms is not enough. To insure that the organisms not
grow and divide within the macrophage, the white cell must kill the
organisms by some means such as the OXIDATIVE BURST.
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Macrophage Attacking E.coli (SEM x8,
800)
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Alveolar (Lung) Macrophage Attacking
E. coli (SEM x10,000)
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宿主介导的免疫反应
The host response to the microorganisms may
be
 protective
 Destructive
 both protective and destructive
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宿主介导的组织损伤
牙周菌斑微生物从生理性组合转为病理性组合，
菌斑的量和质发生变化后，导致牙周组织炎症的
产生。虽然炎症是宿主局限和消除病原物质的防
御反应，但宿主自身组织在这一过程中也会遭到
损伤和破坏。宿主对牙周微生物抗原的各种免疫
应答反应过程中，所产生的生物活性物质具有破
坏作用，不可避免的造成宿主的组织损伤和破坏，
这对牙周病的发生发展有着重要作用。
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宿主介导的组织损伤
（一）非特异性免疫介导的组织损伤
（二）特异性免疫介导的组织损伤
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（一）非特异性免疫介导的组织损伤
包括天然屏障（牙龈上皮）、吞噬细胞（中性粒
细胞和巨噬细胞）及正常体液因素（补体）的作
用。天然屏障具有保护防御功能 ，而后两种因素
则具有防御和破坏的双重作用。
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三、宿主介导的组织损伤
（二）特异性免疫介导的组织损伤
 牙周微生物中，绝大多数是口腔正常菌群。
 正常菌群与宿主的关系极为密切，已经成为一个统一体，
一般不引起宿主的特异性免疫反应。只有当牙周菌斑的量
和质发生改变，即微生物抗原的浓度和性质发生改变后，
才会引起宿主产生特异性免疫反应，包括体液免疫和细胞
免疫两个方面，分别有B、T淋巴细胞承担。
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CHAPTER 3
SPECIFIC BACTERIOLOGY OF
PERIODONTAL DISEASES
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Gingivitis
Nonspecific Gingivitis
Probably affects the whole dentate
population at some stage
The
one periodontal disease that CAN be
ethically studied, since it’s easily reversible
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Studies on gingivitis showed that there
are four phases in its development
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Phases Associated with Experimental
Gingivitis
Phase Time Period
Characteristic Flora
1
0-2 days
Predominantly Gm + cocci
2
2-4 days Increased filaments & fusiform bacilli
3
4-9 days
Increased vibrios & spirochetes
4
10+ days
Gingivitis
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Day
Gm+Cocci
Rods
Gm-Rods
Cocci
Filaments
Gm-vibrios Gingivitis
Spirochetes
0
+
-
-
-
3
+
+
-
-
7
+
+
-
-
10
+
+
+
+
15
+
+
+
+
20
Reinstituted
oral
hygiene
21
+
+
-
+
27
+
+
-
+
30
+
_
-
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Microflora in gingivitis differs from
that in health

An increase (10-20 fold)in plaque mass
Shift from streptococci-dominated-plaque to one in
which Actinomyces spp., capnophilic(especially
Capnocytophaga spp.) and obligate anaerobic
Gm- bacteria predominate

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Hormone-related Gingivitis
Occurs during




Pregnancy
puberty
menstruation
following oral contraceptive use
Not to everyone in these categories， But there is a
hormonal aspect to it
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Prevotella intermedia = major organism involved
P. intermedia requires vitamin K to grow in artificial
media and in vivo may get its vitamin K from othe
r bacteria
These organisms all require vitamin K1 for
growth, Steroid based hormones have chemi
cal structures similar to vitamin K1 and can s
erve as substitutes for vitamin K1
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Hormonal connection: progesterone or estradiol can
substitute for vitamin K
Thus, when these hormones increase, the organism
receives its growth factor
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The significance of this is that the
hormones are elevated
 At
the time of puberty
 During pregnancy
People in these situations may have a gingivitispregnancy gingivitis is the most common
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Acute Necrotizing Ulcerative
Gingivitis (ANUG)





Also described as Vincent’s disease, trench mouth
Rapid onset (1 day)
Characterized by painful, necrotic, ulcerative gingival
lesions ，accompanied by spontaneous gingival bleeding
Possibly accompanied by systemic symptoms including
lymphadenopathy, fever and fatigue.
Psychological or physiological stress or both often present
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Unlike chronic gingivitis, ANUG is a true
infection and microorganisms can be seen
invading the host gingival tissue.
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Organisms frequently found
Prevotella intermedia
Fusobacterium nucleatum
intermediate-sized spirochete (Treponema spp.)
Over the years, other bacteria, and even a virus, have
been found to be elevated
These include Fusobacterium spp., Selenomonas, and Cy
tomegalovirus
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HIV-associated gingivitis
HIV associated gingivitis shows a characteristic linear
erythema at the gingival margin
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Organisms frequently found in HIV associa
ted gingivitis
Candida albicans
 Porphyromonas gingivalis
 Prevotella intermedia
 Fusobacterium nucleatum
 Actinobacillus actinomycetemcomitans
 Campylobacter rectus

They are all opportunistic oral pathogens for the
impaired response in HIV patients
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Periodontitis
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Animal Studies
Socransky monoinfected rats with Gm+
organisms and anaerobic, Gm- organisms,
Results are shown in the next table.
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Effect of Gram-positive and Gram- negative Organisms
on the Periodontium
Plaque
Gram +
Gram -
Bone
loss
Much
Slow
Minimal Rapid
Osteoblasts
Decrease
Normal
Osteoclasts
Normal
Increase
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The hallmark of periodontitis is the loss of connective
tissue attachment to the tooth. Numerous forms of
periodontal disease are found in adult populations,
these forms are characterized by different rates of
progression and different responses to therapy.
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Localized Aggressive Periodontitis
(LAgP)
Several forms of periodontitis are characterized by rapid
and severe attachment loss occurring in individuals during
or before puberty. LAgP develops around the time of
puberty, is observed in females more often than in males.
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Localized Aggressive Periodontitis
(LAgP)




Usually little gingival inflammation
Minimal supragingival plaque
The hallmark of the disease is marked, localized,
rapid alveolar bone loss involving the permanent
first molars and often the incisors
Cases often cluster in families
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This condition is almost uniformly seen in individuals
who demonstrate some systemic defect in immune
regulation, and most affected individuals demonstrate
defective neutrophil function.
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The microbiota associated with localized aggressive
periodontitis is predominantly composed of
capnophilic(CO2 loving) G-anaerobic rods.
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Organisms Frequently Found
in Localized Aggressive Periodontitis
Microbiologic studies indicate that almost all LAgP
sites harbor Aa, which may comprise as much as 90
% of the total cultivable microbiota.
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There are five serotypes(a-e)of Aa. and the virulence
factors produced by Aa are as follows:




Leukotoxin(a protein toxic for polymophs)
LPS(endotoxin, stimulate bone resorption)
Enzymes(degrade collagen)
Aa can invade gingival connective tissue
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Other organisms found in
significant levels include:
P. gingivalis
E. corrodens
C. retus
F. nucleatum
Capnocytophaga spp. and spirochetes.
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Herpesviruses, including EBV-1 and HCMV, also
have been associated with localized aggressive
periodontitis.
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Aa is generally accepted as the primary etiologic
agent in most , but not all cases of localized
aggressive periodontitis . another organism or
organisms are probably involved in some cases
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One study of LAgP in China failed to find A. a. in any
samples from 23 diseased sites in 15 patients but found
a high frequency and proportion of Eubacterium sp(真
杆菌).
In at least the US, Capnocytophaga species are elevat
ed in LAgP and may also play a role in the disease but,
Capnocytophaga gingivalis was among the predomina
nt species in healthy sulci of Chinese patients
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Diagnosed early, this disease responds well to local
treatment and antibiotics that eradicate the diseasecausing bacteria
Studies of therapy indicate that both mechanical
debridement and systemic antibiotic treatment are
necessary to control the levels of Aa in this disease.
The failure of mechanical therapy alone may relate to
the ability of this organism to invade host tissues.
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Tetracycline is effective in eliminating Aa.
and resolving the clinical condition, which is
in contrast to CP when metronidazole might
be chosen because its specific action against
obligately anaerobic bacteria.
Moreover, the combination of metronidazole
and amoxycillin are particularly effective in
LAgP esp. when combined with SRP.
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Generalized Agressive Periodontitis
o
o
o
o
o
Clinical findings are similar to LAgP
Rapid bone loss - except the bone loss is generalize
d rather than localized
Heavy plaque
Observable inflammation
Usually occurs more frequently in young adults
than in children, often beginning with the onset of
puberty
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Predominant Cultivable Flora in Generalized
Agressive Periodontitis
Porphyromonas gingivalis – predominant
Eikenella corrodens
Prevotella intermedia
Capnocytophaga
Neisseria
A. a. is present only in low numbers
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Periodontitis in Juvenile Diabetics
The relationship between diabetes and periodontal
diseases may be bi-directional.
Juvenile diabetics often have more severe
periodontal disease than the general population
Periodontitis begins near puberty and by age 19,
over 1/3 are affected
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Periodontal pathogens may raise pro-inflammatory
mediators that result in insulin resistence and an
increase in blood glucose, thereby predisposing
indidividuals to develop type 2 diabetes. Mechanical
debridement when combined with antimicrobial
agents, can improve glycaemic control.
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Predominant Cultivable Flora in
Periodontitis in Juvenile Diabetics
Capnocytophaga
Pg
Spirochetes
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Chronic Periodontitis
Microbiologic examination of chronic periodontitis
have been carried out in both cross-sectional and
longitudinal studies; the latter have been conducte
d with and without treatment. These studies suppo
rt the concept that chronic periodontitis is associat
ed with specific bacterial agents.
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Microscopic examination of plaque from sites with
CP have consistently revealed elevated proportions o
f spirochetes. Cultivation of plaque microorganisms
from sites of chronic periodontitis reveals high
percentages of anaerobic(90%) G-(75%) bacterial
species.
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Chronic Periodontitis
The organisms associated with CP are shown in
the next table
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Microbiology of CP
Porphyromonas gingivalis
Prevotella intermedia
Bacteroides forsythus
Campylobacter rectus
Fusobacterium nucleatum
Treponema denticola
Eikenella corrodens
Actinobacillus actinomycetemcomitans
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Here you can see a close-up of an agar plate showing the
jet black colonies of these organisms growing from a sub
gingival sample.
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When periodontally active sites(i.e., with recent att
achment loss) were examined with inactive sites sit
es(i.e., with no recent attachment loss), C.retus, Pg,
Pi and Bf were found to be elevated in the active si
tes.
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Furthermore, detectable levels of Pg, Pi ,Bf, C.retus,
and Aa are associated with disease progression, and
elimination of specific bacterial pathogens with therapy
is associated with an improved clinical response.
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Both Pg and Aa have been shown to invade host
tissue cells, which may be significant in aggressive
forms of chronic periodontitis.
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Viral isolates from periodontitis
Recent studies have documented an association
between CP and viral microorganisms of the herp
esvirus group, most notably Epstein-Barr Virus-1
(EBV-1) and human cytomegalovirus(HCMV).
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Viruses have also been found in gingivitis and in
the pockets of periodontitis patients
Human cytomegalovirus (HCMV) was detected in
deep periodontal pockets of two chronic and two
localized Aggressive periodontitis patients but not
in any shallow periodontal sites
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HCMV - is the virus most often found
Also found
Epstein-Barr Virus
Herpes
Simplex Virus
Human
Papillomavirus
Human
Immunodeficiency Virus
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Further, the presence of subgingival EBV-1 and
HCMV are associated with high levels of putative
bacterial pathogens, including Pg, Bf, Pi, and T. dentic
ola. These data support the hypothesis that viral
infection may contribute to periodontal pathogenesis.
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These viruses can infect host cells, including PMN,
macrophages, and lymphocytes, and they induce
the expression of potenially tissue-damaging
cytokines and chemokines.
It is proposed that these viruses could reduce the
effectiveness of the local host defences, thereby
giving certain subgingival bacteria the opportunity
to escape from homeostasis and reach clinicallysignificant levels.
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Refractory chronic periodontitis
Treatment of chronic periodontitis by conventional
methods is usually effective. However, in a small
subset of patients therapy fails to stop progression of
disease despite excellent patient compliance.
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Patients who have unexpectedly not respond to
therapy are referred to as having refractory
periodontitis. In fact, patients who are given this
diagnosis represent a very heterogeneous group
clinically and microbiologically.
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The microflora taken from progressing sites in
some of these patients is usually diverse and may
contain rods, and Candida.
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In other patients, persistently high levels are
found of one or more of the following bacteria:
Pg, Bf, Pi, Eikenella corrodens. From a microbi
ological point of view it is clear that refractory
chronic periodontitis is not a single entity.
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Chronic periodontits patients with refractory disease
are candidates for microbial testing to identify sub
gingival bacteria that might be responsible for the
continuing infection. In such cases, one to two paper
points are inserted into representative therapyresistant pockets for approximately 20 seconds, with
drawn, and immediately placed in reduced transport
fluid, and then sent to a licensed clinical laboratory
for analysis.
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Cultivable putative pathogens are identified and their
sensitivity to various antibiotics determined. Clinicians
can use the laboratory report as a guide for possible
adjunctive antimicrobial therapy in treating the patient’s
refractory periodontitis. Cultural analysis and antibiotic
sensitivity testing are not done in most cases of chronic
periodontitis because the disease usually responds to
conventional therapy.
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Sampling deepest pockets with a paper point
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Laboratory processing of bacterial samples
with DNA probes
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Periodontal abscess
Periodontal abscesses are acute lesions that may
result in very rapid destructions of the periodontal
tissues.
They often occur in patients with untreated
periodontitis but also may be found in patients
during maintenance or after scaling and root planing.
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Periodontal abscesses also may occur in the absence
of periodontitis, for example, associated with impaction
of a foreign object (e.g., a popcorn kernel or dental floss)
or with endodontic problems.
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Inflamed marginal and papillary gingiva adjacent to an
overcontoured porcelain-fused to metal crown on the
maxillary left central
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Inflamed gingiva and deep probing depth in
maxillary central incisors
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A full-thickness mucoperiosteal flap has been
reflected to expose the elastic ligature
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Typical clinical symptoms of periodontal abscesses
include
pain,
swelling,
suppuration,
bleeding on probing,
and mobility of the involved tooth.
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Signs of systemic involvement may be present,
including cervical lymphadenopathy and an elevated
white blood cell count.
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Periodontal abscess




Occurs with pre-existing periodontitis
Acute infection
Occurs in the walls of periodontal pockets as a res
ult of the invasion of bacteria into the periodontal
tissues
More common in periodontitis patients with a syst
emic disease such as diabetes
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Investigations reveal that bacteria recognized as
periodontal pathogens are commonly found in
significant numbers in periodontal abscesses
These microorganisms include ：
Fn, Pi, Pg, Bf
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Periodontitis as a manifestation
of systemic disease
Previous classification schemes delineated “prepubertal
periodontitis” as a rare form of periodontitis found to
affect the primary dentition.
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This group has now been reclassified under the
heading of periodontitis as a manifestation of
systemic disease because most children with
severe periodontal destruction also demonstrate
profound immunologic abnormalities.
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The underlying immune deficiency may vary and
includes neutrophil defects and leukocyte adhesion
defects, for example, recent studies have demonstr
ated that some cases of severe periodontal destructi
on are associated with a mutation in the cathepsin
C gene in afflicted children.
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Studies of patients with “prepubertal periodontitis ”
indicate that subgingival bacteria associated with
other forms of periodontal disease also are found in
these patients.
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This is consistent with the concept that the occurrence
of severe destruction at an early age is a reflection of
an increased host susceptibility, in this case resulting
from systemic disease. Identification of severe
periodontal destruction may be one of the first signs
of systemic diseases.
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掌趾角化－牙周破坏综合征
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NEUTROPHILS
in all inflammatory lesions
chemically attracted to area through
chemotaxis
tissue destruction because of
substances in their granules
leukocyte abnormalities can lead to
more severe periodontal disease
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5-year-old boy with cyclic neutropenia, note the
aggressive and extensive inflammation
in gingival tissues
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7-year-old boy with cyclic neutropenia demonstrating
acute and extensive gingival inflammation and advanced
attachment loss
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Clinical appearance of patient with leukocyte adhesion
deficiency, the tissue inflammation is evident
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The extensive bone loss
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A patient with leukocyte adhension deficiency, the
patient suffered from recurrent infections of the
middle ear, tongue and periodontium.
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Radiographic appearance
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In general, Gram-negative, anaerobic microorganis
ms are the principle bacteria associated with most p
eriodontitis diseases
The most commonly identified so far are shown in t
he next table
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Gram-negative Bacteria Causing
Periodontal Diseases
Porphyromonas gingivalis
Prevotella intermedia
Bacteroides forsythus
Campylobacter rectus
Actinobacillus actinomycetemcomitans
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These are thought to be the most important
because
they have been found in large numbers during
active disease
they have been shown to possess a number of
virulence factors
Other bacteria found in lower numbers may be
important but have not been studied to the same
extent as these
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