MILITARY MEDICINE, 166, 1:085,2001
Periodontal Disease and Its Association with Systemic Disease
Guarantor: Edward B. Fowler, DDS MS*
Contributors: Edward B. Fowler, DDS MS*; Lawrence G. Breault, DMD MSt; Michael F. Cuenin, DMD*
Periodontal diseases are oral disorders characterized by in-
flammation of the supporting tissues of the teeth. Usually,
periodontitis is a progressively destructive loss of bone and
periodontal ligament (loss of the attachment apparatus of the
teeth). Periodontitis has documented risk factors, including
but not limited to specific plaque bacteria, smoking, and dia-
betes mellitus. Initially, the link between systemic disease and
periodontal diseases was thought to be unidirectional. Cur-
rently, there is increasing evidence that the relationship be-
tween these entities may be bidirectional. Recent case-control
and cross-sectional studies indicate that periodontitis may
confer a 7-fold increase in risk for preterm low birth weight
infants and a 2-foldincrease in risk for cardiovascular disease.
These early reports indicate the potential association between
systemic and oral health. Additionally, these studies support
the central hypothesis that periodontal disease involves both a
local and a systemic host inflammatory response. This knowl-
edge of disease interrelationships may prove vital in interven-
tion strategies to reduce patient risks and prevent systemic
disease outcomes. Based on the current evidence of the peri-
odontal-systemic disease connection, the purpose of this re-
port is to help establish the groundwork for closer communi-
cation between physicians and periodontists in the military
health care setting.
Introduction
E vidence-based clinical medicine requires that all clinicians
consider patient risk factors on a daily basis in terms of
disease assessment, diagnosis, and therapeutic outcomes. Of-
ten, health care providers lntuitlvely weigh patient risks for
developing disorders and use that information to make treat-
ment decisions or recommendations. As providers seek guld-
ance in decision making, they may encounter conflicting infor-
mationpublishedin the professional literature. Onestudy may
support a genetic profile, behavior, or exposure as affecting the
risk for a disorder, and another may refute this association. In
dentistry, there has been a significant increasein citationsdeal-
ingwith disease risk, especially related to periodontal diseases.
A number of recent studies have provided evidence suggesting
that periodontitis may increase the risk for systemic disorders
such as cardiovascular diseases and premature birth of low
weight infants.1-4 This report was written to serveas a resource
for military health care professionals to assess and use the
current evidence on periodontal-systemic disease risk associa-
tions.
*Chief ofPeriodontics, DENTAC FortLewis, Washington.
tChief ofPeriodontics, DENTAC Hawaii.
*Director, U.S. Army Periodontic Residency Program, FortGordon, GA.
This manuscript wasreceived for review in December 1999 and wasaccepted for
publication in February 2000.
Reprint & Copyright © byAssociation ofMilitary Surgeons ofU.S., 2001.
85
The Natural History of Periodontal Diseases
Periodontal diseasesare prevalent disorders withrisk param-
eters that contribute to morbidity in terms of decreasing oral
function and increasing tooth loss." Risk factors have been
studied extensively in dentistry and include specific bacteria,
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smoking, and systemic diseases such as diabetes mellitus."?
Genetic factors, whichare based on polymorphism and inflam-
matoryresponses, have also been tdentifled.s" It has been esti-
mated that approximately one-thirdof adults are afflicted with
someform ofperiodontitis. 10-12 Advanced destruction from this
inflammatory diseaseaffects one ofevery eightindividuals, with
an increase in prevalence to one of every three persons by the
age of 55 to 65 years. Symptoms of periodontal diseases are
generally insidious, but as the destructive .Inflammatton
progresses, gingival discomfort or tenderness, tooth mobility or
looseness, gingival abscesses, and/or tooth loss oftenoccur.
The central pathophysiologic event in the natural history of
periodontal diseaseis chronic exposure to pathogenic oralflora.
Etiologic bacteria that have been implicated in periodontitis
include Porphyromonas gingivalis, Actinobacillus actinomyce-
temcomitans, Bacteroides jorsythus, and Treponema denti-
cola. 13,14
Dental plaque is a matrix-enclosed environment in which
pathogenic bacteria coexist. This plaque functions as a micro-
bial biofilm that exposes the host to bacterialcellsurface com-
ponents such as lipopolysaccharide (LPS). LPS and other bac-
terial products can penetrate the tissues within the gingival
sulcus. In these locations, host defense cells (monocytes and
macrophages) come in contact with the bacterial components.
LPS can form complexes withbindingproteinson the surfaceof
the host defense cells. Thisresults in bindingto CD 14receptors
on monocytes and macrophages, an event that leads to the
expression and releaseoflocal immunoinflammatory mediators
such as cytokines and arachidonic acid metabolites." These
biochemical and cellularinteractionsheraldthe histologic onset
ofperiodontal disease, whichcan result in destructionoftissue
and attachment IOSS.16
Thecentralhypothesis of"periodontal medicine" is that infec-
tions from periodontitis present as a chronic inflammatory bur-
den at a systemic level. 17 At various times throughout history,
the concept that infections of the mouth could influence sys-
temic health has been debated. Miller originally described this
focal theoryofinfection in 1891 "since microorganisms or their
waste products obtain entrance to parts ofthe bodyadjacent to
or remote from the mouth.?" Miller listedthe following diseases
as having their origins from oral relationships: (1) pneumonia,
(2) tuberculosis, (3) syphilis, (4) meningitis, and (5) septicemia.
Hunterblamed"oral sepsis" forinitiating tonsillitis, infections of
the middle ear, glandular swellings, empyema, meningitis, os-
teomyelitis, and ulcerative endocarditis.'? Before the develop-
Military Medicine, Vol. 166, January 2001
86 Periodontal Disease and Its Association withSystemic Disease

ment of modem periodontal treatments, during the three de-
cadesfrom 1910to 1939, manyteethwere extracted prophylac-
tically because of the focal infection hypothests.P:" Cecil and
Angorine followed patients with rheumatoid arthritis and re-
ported that none improved after full mouth extractions." Then
in 1952, an editorial in the Journal of the American Medical
Association stated that "many patientswithdiseases causedby
foci of infection have not been relieved of their symptoms by
removal of the foci. Many patients with these same diseases
have no evident focus of infection; also, foci ofinfection are asnary tract tnfecttons." Vaginal colonization with Bacteroides
common in apparently healthypersonsas thosewith disease.?"
Subsequently, the focal theory ofinfection was not significantly
revisited for the next 50 years.
PLBW.33 Long-term disorders associated withPLBW include ce-
rebral palsy, respiratory distress, and learning disabilities.
Although prenatal care interventions are widespread in the
United States, infant mortality rates have not diminished sig-
nificantly in the recent past. Known risk factors for PLBW in-
cludedrug, alcohol, and tobacco use, low socioeconomic status,
inadequate prenatal care, hypertension, diabetes, African-
American race, maternal age younger than 17 years or older
than 34 years, history of multiple pregnancies, and genitouri-
species increases PLBW rates by 40 to 60%.35-37 It has been
reported that between 18 and 49% ofinflamed chorioamnionic
membranes havenegative bacterial cultures." Asa result, it is

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Mattila et al utilized sound scientific methods to reintroduce
the association between systemic disease and oral infection. 1 theorized that translocation ofbacterial products, such as LPS
Epidemiologic studies supported the concept that periodontal from the vaginal tract or maternally produced inflammatory
disease maybe a separaterisk factor for cardiovascular disease mediates, may cause PLBW indtrectly."
and premature low birth weight tnfants.>" In light of these The concept that periodontal infection could mediate PLBW
findings, Offenbacher coined the term"periodontal medicine" as indirectly was first tested on a hamster model." Results indi-
a discipline that studies the relationship between systemic dis- cated that animals receiving live P. gingivalis had a 15 to 18%
ease and periodontitis. 15 Offenbacher hypothesized that decrease in fetal weight. Furthermore, pretreatment with heat-
through randomized clinical trials completed during the next killed bacteria did not result in protection against lower fetal
decade or two, periodontal medicine concepts will guide clini- weights. The low-grade infections that were produced in these
cians in making evidence-based decisions to improve both the hamsters did not induce malaise or fever but did result in in-
oral and systemic health ofpatients. creased prostaglandin E2 (PGE2) and tumor necrosis factor-a in
The basis for considering oral infections as being involved inobtained aspirates. Collins et al." tested the effects of experi-
systemic disorders derives from the microscopic aspects of in- mental periodontitis on pregnant hamsters. They determined
flammatory periodontal disease progression. As the integrity of that animals that exhibited experimental periodontitis had sig-
the epithelium ofa periodontal pocket is violated, not only can nificantly smaller meanlitterweights. Furthermore, these same
bacterial productsenterunderlying host tissues,but whole bac- animals had significant increases in intra-amniotic fluid con-
teria can enter as well." Additionally, certainbacteria, such as centrations ofPGE2and tumornecrosis factor-a compared with
P. gingivalis and A. actinomycetemcomitans, possess virulence animals without experimental periodontal infections. These im-
factors that allow for directinvasion ofintact tissues." Subse- munoinflammatory mediators are known to induce cervical di-
quently, patients are exposed to transient bacteremias, even lation, uterine contraction, labor, and spontaneous abortion."
with normal daily functions such as chewing and tooth Offenbacher and coworkers' determined, in a case-control
brushing. 27-29 The exposure to LPS and otherbacterial products studyof124pregnantand postpartummothers, that PLBW was
can trigger mediator expression and the sequence of events of associated with more clinical attachment loss than cases of
inflammation. This mayhave consequences on organ systems of normal birth weight. After adjusting for otherknown riskfactors
the body. Prostaglandins causeoxidative stress, oxidation oflow- such as alcohol use, tobacco, and maternal age, there was a
density lipoprotein, and contraction ofsmooth muscle. Similarly, significant and strong association between periodontal disease
cytokines can stimulate endothelial adhesion, metabolic wasting, (attachment loss ~3 mm at 600iD of sites) and PLBW. The ad-
hyperlipidemia, connective tissue catabolism, and release of justed odds ratio was 7.5 to 7.9.
acute-phase proteins. IS Many of these have been implicated in Offenbacher et al.," in a follow-up human study, determined
systemic diseases. Slade and coworkers" analyzed the data from the differences in local host response and oralflora. Theresults
the third National Health and Nutrition Examination survey and ofthis case-control studyindicated that gingival crevicular fluid
levels of PGE2were significantly greaterin mothers with PLBW
found significant increases in serumC-reactive protein in patients
with periodontitis. These data indicate that systemic release of compared with women with normal birth weight infants. Fur-
inflammatory markers occurs in response to periodontal inflam- thermore, it was noted that smaller and more preterminfants
mation. were born to women with higher gingival crevicular fluid-PGE 2
levels. In addition, periodontal pathogens (A. actinomycetem-
Periodontal Diseases and Preterm Low Birth Weight comitans, P. gingivalis, B.forsythus, and T. denticola) were found
at increased levels in PLBW mothers, but these differences were
Preterm low birth weight (PLBW) is defined when a birth not statistically significant compared with women with normal
occurs before 37 weeks ofgestation and the infant weighs less birth weight infants.
than 2,599g.31 In the United States, PLBW has a 10% incidence Offenbacher's group" recently compared blood samples from
annually. Additionally, PLBW accounts for 60% of all infant fetal cords for the presence of immunoglobulin (IgM)-specific
mortality that is not the result of anatomic or chromosomal antibody againstvarious periodontal pathogens. In PLBW sam-
congenital defects." PLBW has a significant impacton society in ples, 33.3°iD tested positive for IgM directed against the tested
terms ofeconomics and morbidity. It is estimated that $5 billion bacteria, compared with 17.9°iD ofnormal birth weight samples.
is spent annually for infant intensive care in the treatment of Ofthe 13 different tested periodontal pathogens, IgM was more

Military Medicine, Vol. 166, January 2001

Periodontal Disease and Its Association with Systemic Disease
often encountered against Campylobacter rectus, P. gingivalis,
and Fusobacterium nucleatum Although both pretermand nor-
mal birth weight infants had fetal cord IgM directed against
specific bacteria, these fetal immune responses indicate that
maternal periodontal infections can provide a systemic chal-
lenge to the fetus in utero.
As a result of the Offenbacher studies, it is proposed that
periodontitis can be associated with premature births. Peri-
odontal infections remotely seedbacteria, LPS, and othermedi-
ators into the systemic circulation. These can stimulate a local
release ofinflammatory mediates at the fetus, which maycause
cervical dilation, cervical effacement, contraction, and preterm
delivery. Dr. Marjorie Jeffcoat is completing ongoing researchat
the University ofAlabama in Birmingham; the results of these
studies should elucidate this relationship further.
Periodontal Diseases and Cardiovascular Disease
Fourteen million (20%) of all annual deaths are caused by
cardiovascular disease." Cardiovascular disease is the major
cause ofdeath in developed countries. Atherosclerosis (acondi-
tionconsidered synonymous withcardiovascular disease) is the
result offibrolipid deposition in the intimaoflarge and medium
arteries. When severe, this progressive, chronic disease leadsto
reduction ofthe lumenofthe blood vessels and predisposes the
individual to obstruction, thrombosis, and ischemia. The disease
may present itself as coronary heart disease or cerebral vascular
accidents and can even precipitate a myocardial infarction.
There are multiple similarities between patients with peri-
odontitis and cardiovascular disease. Bothare associated with
males, older populations, higher stress levels, lower levels of
education, and tobacco use." In patients with periodontitis,
cardiovascular disease is the most common systemic disor-
der.46,47 The relationship between these two diseases was indi-
rectly evident in early studies. It was noted that oral infections
occurred more often in males with strokes compared with age-
and community-matched controls." Increased markers for
thrombosis (fibrinogen and white blood cell counts) correlated
with a patient's gingival index (and indicator of periodontal
health)."
Mattila's group' initially noted the association between peri-
odontal disease and cardiovascular disease in 1989. Theirfirst
study reported that the association of poor dental health and
myocardial infarction had an odds ratio of 1.3. In other words,
patients with poor dental health were 1.3 times more likely to
have had a myocardial infarction than patients with good oral
health. In that series of studies, oral infection included caries,
endodontic conditions, and components ofperiodontal disease.
The relationship between oralhealthand cardiovascular disease
occurred independent of known risk factors such as smoking,
hypertension, diabetes, total cholesterol, triglycerldes, and age.
In a subsequentstudy by Mattila and coworkers/" there was
an association between dental index scores and narrowing of
coronary arteriesin males (odds ratioof1.4), but no association
wasfound in females. While monitoring newmyocardial infarc-
tionsduring a 7-yearperiod, Mattila's group" furthernotedthat
individuals with poordental indexscores had a hazard ratio of
1.2. One must be aware that the total dental index reflects not
only periodontal infections but also other oral infections that
maybe discrete and independent.
87
In the first longitudinal National Health and Nutrition Exam-
inationSurvey, DeStefano et al.2 assessed periodontitis with a
periodontal index. They reported that patientswithperiodontal
disease had a 250/0 increased risk for coronary heart disease
compared with patients with minimal disease. After adjusting
for potential risk factors, in malesyounger than 50 years peri-
odontitis had a relative risk of 1.72for coronary heart disease.
While studying the Gila River Indian Community, Genco and
coworkers" determined that individuals older than 60 years
with periodontal bone loss were 2.68 times more likely to de-
velop cardiovascular disease (after adjusting for gender and
duration ofdiabetes). Joshipura et al.53 stratified tooth loss by
periodontal history and notedin males withperiodontal disease
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that therewasa significant relative risk ofmyocardial infarction
before age 60 years.
Studiesfrom the University ofNorth Carollna'' notedthat even
after adjusting for known risk factors, high alveolar bone loss
scores were associated with incidence odds ratios of 1.5, 1.8,
and 2.8 for total coronary heart disease, fatal coronary heart
disease, and stroke, respectively. Asseverity ofboneloss scores
increased, so did the cumulative incidence of these three out-
comes from cardiovascular disease. Theauthors concluded that
their findings support the concept that exposure to periodontal
infection follows a dose-effect relationship with cardiovascular
disease.
Another study by this group" defined periodontal disease by
attachment loss. They noted significantly more periodontal de-
structionin patients with coronary heart disease and subclini-
cal atherosclerosis compared with healthycontrols.
Recent studies55,56 have reported that Streptococcus sanguis
and P. gingivalis can express a collagen-like platelet aggrega-
tion-associated protein that can stimulate thrombosis. Genco
and coworkers" suggested that patients with P. gingivalis in
periodontal pockets had an oddsratioof2.8 for having myocar-
dialinfarction. Zambon et al.58 isolated DNA sequences ofperi-
odontal pathogens from human atheromas. Tofurther support
an infectious cause for cardiovascular disease, other nonperi-
odontal infectious agents (Chlamydia pneumonia, Helicobacter
pylori, cytomegalovirus, and herpes simplex virus) have been
detected in atheromas.
Although atheromas and thrombosis are independent events
in patients, these may be exacerbated by systemic LPS and
microbial exposures posed by periodontal disease. As a result,
periodontitis mayinfluence platelet aggregation, atherogenesis,
and the formation ofthrombi. Ifthis occurs, the risk ofathero-
sclerosis, stroke, and coronary heart disease also would be
increased. 17
Summary
This review reports that studies are currently associating
periodontal infections withcardiovascular disease and preterm
low birth weight. Cumulative data suggest that patients with
periodontal disease are seven timesmore likely to bear prema-
ture low birth weight infants and twice as likely to havecardio-
vasculardisease. It is not known if there is a directcause-and-
effect relationship. Furthermore, it is not known ifthe treatment
ofperiodontitis can prevent the incidence ofthese two systemic
conditions. It has beendemonstrated, however, that periodontal
treatment can decrease serum levels of C-reactive protein,
Military Medicine, Vol. 166, January 2001
88
which is an acute-phase reactant produced by the liver in re-
sponse to tnflammatton." Decreasing the serum level of C-re-
active proteins is associated withreduction in the risks ofmyo-
cardial infarction. 61 Thus, the hypothesis that periodontal
treatment can potentially reducethe risk ofsystemic disease is
indirectly supported.
Further studies in the new field of periodontal medicine are
ongoing. It is importantthat health care providers be aware of
these data and provide their patientswithcurrent and accurate
information on the potential relationships between periodontal
diseasesand systemic conditions. This information is probably
more significant to patients with other known risk factors (fa-
milial history, diabetes, smoking). 17 It is appropriate for medical
and dental colleagues to work together and share knowledge so
that the appropriate diagnosis and treatmentcan be provided to
patients. Ultimately, improving oral health might not only im-
prove quality oflife from a dental standpointbut mightreduce
the risk ofsystemic disease as well.
The goal of overall improved patient wellness requires that
military and civilian medical and dental communities work in
concert in this pursuit.62 For those clinicians wishing to review
the interrelationship between periodontal disease and systemic
disease further, a recentconference at Chapel Hill, North Caro-
lina, resulted in the publication of the third volume of the An-
nals of Periodontology. 63
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I AMSUS Medals and Insignia Wearing the Association Ribbon I
. . . . .. The Act of Congress of emonies and functions of I
I Designed exclusively for theassociation of Military Surgeons ofthe U.S., these January 30. 1903. that incor- such societies, and they may
I official medals and insignia are authorized by Congress to be worn by members. porated the Association , car- then be worn with decora-I
. . . . . ried in section 3 th e follow- tions, service medals, or sub- I
I Association emblems appearing on the medals and mngrua illustrate gold ing words: "That the said As. stituted therefore."
finish with hard-fired enamel colors ofred, white and blue. sociation ... may adopt a seal There the matter stands. I
Qty. Item Price and insignia wh ich may be The Association feels that the I
Small Medal $8 .00 worn by its members." Act of Congress governs, and I
La I B $500 As the membership was thatthe wearing of the ribbon
- ~e Ma:d~".·.·.·.·."$1 1.00 made. up at that time en~irely ~pon the uniform at any time I
- 'bOO .2 00 of uniformed personnel It ap- IS legal , and many command- I
Ri n .Fro nt . pears incontestable ing officers have seen no im-
_ ~pe~ Pin $6 .00 that th is authorization was for propriety in that artitude. On I
T~e Pin ;; : $6 .00 the wearing of the insignia the other hand the will of the I
Tie Tac I Cham $6 .00 (th e ribbon) upon the uni- commanding officer is final in
form and there is no limita- the matter of the uniform. Hell
_TOTAL .... $_ _ tion on its wearing contained she may ban the ribbon of the I
110 minimum on credi t card in this Act of Congress. Association as helshe may any
orders
It is clearly not within the other item , and hiszher orders I
please make checks payable to power of service regulation to may be questioned only I
Medals a re shown smaller tban actUal size
AMS US set aside an authorization through the usual procedures I
granted by th e Congress . and after his/her orders have
Payment by: Ocheck OMasterCard OVisa OAmerican Express How ever from the office of been obeyed . Perhaps th e I
th e Adjutant General of the time will come when thi s veX-I
Credit Card Number: Exp. _ /_ Army has come the following ing question can be settled in
Signature: _ decision : a Fed eral court. I
"Badges of societies will be I
wo rn on the uniform only
Member Number: OThis is an ad d ress change. Please update when attending meetings, cer- I
Name Order From: Membership Department I
Rank Corps Service AMSUS I
S 9320 Old Georgetown Road I
treet Bethesda, MD 20814
LCity State Zip or fax to: 301.530.5446 ~
I

Military Medicine, Vol. 166, January 2001