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STRESS AND INFLAMMATION IN PERIODONTAL

Review Articles
DISEASE: A REVIEW OF THE BASIC BIOLOGICAL
MECHANISMS
Oriola Madhi1a* , Rozarka Budina1b , Blerta Rumano1c
1
Department of Periodontology and Conservative Dentistry, Faculty of Dental Medicine, University of Medical Sciences, Tirana, Albania

a
DDS, PhD Student, Clinical Professor; e-mail: madhi.oriola@gmail.com; ORCIDiD: https://orcid.org/0000-0002-0958-1214
b
DDS, PhD, Professor; e-mail: zarkabudina@yahoo.com; ORCIDiD: https://orcid.org/0000-0003-0694-1728
c
DDS, MSc, Clinical Professor; e-mail: b.rumano@yahoo.com; ORCIDiD: https://orcid.org/0000-0002-9686-0878

ABSTRACT https://doi.org/10.25241/stomaeduj.2020.7(2).art.5

Background Periodontitis is a multifactorial infectious disease influenced by a myriad of other conditions
and factors amongst which, psychosocial stress has emerged as a potential risk indicator. In order to establish
this link in a generally accepted theory, we need to better understand the physiological pathways of stress
on immune response with implications in the periodontal disease.
Objective This article aims at synthesizing the current knowledge on the effect of the psychological factors
on the periodontal disease and to provide an insight into the bidirectional links between stress-related
disorders and periodontitis via psychoneuroimmunology studies.
Data sources A search was performed in 2 databases - PubMed and Google Scholar, supplemented by a
manual search in peer-reviewed journals and cross-referenced with the articles accessed. The key terms used
were: periodontal disease, periodontitis, stress, psychosocial stress, inflammation.
Study selection The inclusion criteria were all published potentially relevant articles on relationship
between stress, inflammation and periodontitis on human and animal models. The exclusion criteria were
articles with non-available full text and articles that were not written in English.
Data extraction Two reviewers extracted information regarding the quality and study characteristics
independently. The studies were assessed for their methodology, statistical analysis, characteristics of the
periodontal outcome measures, and psychological measurements.
Data synthesis Considerable evidence documents the link between psychosocial stress and periodontitis.
This should redirect the attention of researchers and clinicians towards a multidisciplinary approach
to periodontitis where psychosocial disturbances might be a key component into the rebus of disease
progression and treatment results.
KEYWORDS
Periodontitis; Stress; Psychosocial Stress; Inflammation; Glucocorticoids.

1. INTRODUCTION play, no isolated factor could solely explain the
tissue destruction phenomenon [4]. The concepts of
Periodontitis is a chronic inflammatory condition periodontal disease etiology have evolved towards
affecting the supporting tissues of the teeth, which understanding the role of the immune system and the
results in loss of connective tissue and bone support inflammatory reaction in defining the host response.
and is a major cause of tooth loss in adults [1]. The Those components do play an important role in the
advanced form of the disease affects a smaller part progression of the periodontal disease, which is
of the adult population, around 7% to 15% [2] while further influenced by genetic and environmental risk
milder to moderate forms of the disease are found in factors [5]. Some of the genetic disorders may alter
approximately 50% of the population [3]. the host immune response which could predispose
Its etiopathogenicity is complex with many factors individuals to severe periodontal destruction. They
interplaying, and due to this dynamic interrelated might affect the production or function of polymor-

OPEN ACCESS This is an Open Access article under the CC BY-NC 4.0 license.
Peer-Reviewed Article
Citation: Madhi O, Budina R, Rumano B. Stress and inflammation in periodontal disease: a review of the basic biological mechanisms. Stoma Edu J.
2020;7(2):117-122.
Received: April 28, 2020; Revised: May 13, 2020; Accepted: May 21, 2020; Published: May 26, 2020
*Corresponding author: Dr. Oriola Madhi, DDS, PhD student, Clinical Professor, Klinika Stomatologjike Universitare, QSUT, Rruga e Dibres, Tirane, Albania
Tel/Fax: +355692077065; e-mail: madhi.oriola@gmail.com
Copyright: © 2020 the Editorial Council for the Stomatology Edu Journal.

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phonuclears (PMN), which are known to play a levels. The studies served to provide evidence on the
Review Articles pivotal role in the defense against bacteria. As association between immune response and stress
a result, individuals suffering from neutropenia, components in a cellular and molecular level. The
agranulocytosis, Chédiak–Higashi syndrome exhibit periodontology clinical studies were assessed based
more severe forms of periodontitis due to impaired on the criteria used to define periodontal disease,
immune response. In leukocyte adhesion deﬁciency adjustment for confounding factors, psychometric
(LAD) syndromes, neutrophils lack specific pro- instruments, and the stress markers that were used
teins which allow them to adhere to vessel walls to evaluate the stress component.
and effectively migrate to the infection site. As a The articles included used parameters to define the
consequence, periodontal tissue destruction advan- periodontal disease, such as bleeding on probing,
ces due to an impaired immune defense [6]. While probing depth, recession level, attachment loss,
this is clear evidence of how a deficient host response alveolar bone loss and missing teeth.
might affect periodontal disease, other conditions The stress component was evaluated through
associated with exaggerated immune response are psychometric instruments such as questionnaires
thought to also affect the disease. or stress biomarkers such as salivary cortisol levels,
In this light, psychosocial stress has emerged as a risk crevicular interleukin levels, or urine corticosteroid
indicator with several studies documenting a positive levels.
relationship between psychosocial stress and forms
of the periodontal disease [7]. 3. RESULTS
As the scientific evidence is now unequivocal on the
effects of psychological stress on immune systems The review identified the following noteworthy
and other systemic conditions through a network aspects related to stress, inflammation and perio-
of pathways, it would be reasonable to also explore dontitis visible on human and animal models:
periodontitis and its relations to stress under this
paradigm. 3.1. Stress and periodontium
Stress, can be defined as a set of emotions, triggered
2. MATERIALS AND METHODS by an actual or perceived threat, giving rise to physio-
logical and psychological changes [8]. As the
A literature search was conducted for relevant psychological aspects get reflected in a set of beha-
studies addressing the issue of the relationship vioral reactions that redefine one’s priorities, the oral
between stress, inflammation and periodontitis hygiene habits change for the worse, new patterns of
undertaken on human and animal models. Data avoidance emerge together with substance abusive
sources: A search was performed in 2 databases- behaviors such as smoking and alcohol consumption
PubMed and Google Scholar, supplemented by a [9-10]. On the other hand, physiological response
manual search in peer-reviewed journals and cross- that the body compiles in reaction to stressful stimuli
referenced with the articles accessed. The key terms which are perceived as threats, affects the immune
used were: periodontal disease, periodontitis, stress, system and alters the host defense as a consequence.
psychosocial stress, inflammation. Study selection: Stress association to periodontal disease has been
The inclusion criteria were all published potentially suggested for more than 50 years and the evidence
relevant articles on relationship between stress, in favor of this putative relation has been growing
inflammation and periodontitis conducted on with different studies.
human and animal models. The exclusion criteria Necrotizing ulcerative gingivitis (NUG) was the first
were articles with non-available full text and articles disease to be investigated in relation to stress, for
that were not written in English. Studies published in its acute infectious etiology caused by bacteria that
dental and medical journals were included together are non-pathogenic under normal oral conditions.
with a selection of studies from psychology literature. Under these circumstances it would be reasonable to
The studies were assessed for their methodology, search for host defense alterations that would cause
statistical analysis, characteristics of the perio- the outbreak [11].
dontal outcome measures, and psychological In a study exploring the effect of stress on NUG, by
measurements. measuring the corticosteroid levels in the patient’s
The psychoneuroimmunology (PNI) studies were urine, the NUG cases did exhibit higher levels of the
classified into intervention studies which evaluate stress marker in the urine samples, yielding a positive
the immune response after exposure to intervention correlation as hypothesized [12].
(e.g. relaxation or hypnosis) and vulnerability studies Earlier studies looking for a correlation between
which asses the functioning of the immune system psychological stressful periods such as exam seasons
in association with psychological vulnerability. These in college students and the rate of NUG also showed
studies used inflammatory mediators or markers of a higher incidence of the disease in the sample [13].
inflammation to assess the immune response to stress, The literature has provided robust evidence supp-
including mainly natural killer cell activity, cytokine orting the hypothesis of stress being a predisposing
production, glucorticoid levels and chatecolamine factor in NUG, through immunological mechanisms.

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3.2. Periodontium and other systemic conditions between the actual or perceived stimuli and one’s

Review Articles
Periodontitis as an oral inflammatory disease, can stress response, neuroendocrine and biochemical
induce minor systemic inflammation through markers changes that follow can lead to adverse effects on the
of inflammation like interleukin 6 (IL-6) and C-reactive proper functioning of the immune system [21-22]. In
protein and the spread of lipopolysaccharide (LPS) trying to understand the pathways through which
and flagellin from its causing bacteria into systemic stressors translate into a physiological response from
circulation [5]. There is growing evidence that perio- the immune system, endocrine and nervous system, a
dontitis induced inflammation can further lead growing body of evidence has been mounted through
to neuro-inflammation through the activation of studies and experiments in the field of psychoneuro-
microglia, which are brain immune cells [14]. immunology.
The results of a recent clinical study conducted A synthesis of the main theories deriving from this
on over 60000 participants, support the theory of work is presented below, aiming at elucidating the
elevated systemic inflammation being associated link with implications in periodontal disease.
with stress related disorders such as depression. According to a theoretical study by G. Slavich [23]
The study revealed a significantly higher incidence “Two physiological pathways are responsible for
rate of subsequent depression on periodontitis converting social-environmental adversity into
patients compared to the control group, suggesting broad pro-inflammatory transcriptional programs.
that periodontitis may increase the risk of subse- The first pathway involves the sympathetic nervous
quent depression and can be considered an system (SNS), and the second pathway involves the
independent risk factor regardless of sex, age, and most hypothalamic–pituitary–adrenal (HPA) axis” [24].
comorbidities [15]. Furthermore, new clinical data
support the evidence that increased systemic infla- 3.4. Sympathetic nervous system
mmation is associated with stress-disorders including Stressful stimuli elicit a response from the autonomic
depression. In a recent study, the authors measured nervous system, in the form of catecholamine secre-
the activity of microglia brain cells and showed that tion. The sympathetic branch of ANS responds by
patients had increased levels of neuro-inflammation releasing norepinephrine into lymphoid organs and
during depressive episodes when compared to a vasculature and perivascular tissues, altering the pro-
healthy control group. They concluded that there is inflammatory cytokine levels. The neurotransmitter
incentive to evaluate anti-inflammatory therapies in then, reacts directly on the β-adrenergic receptors
major depressive disorder [16]. Besides this, studies and provokes the due changes on the immune system
conducted from a psychosocial perspective suggest components through signaling transcriptional mess-
that periodontitis could be contributing to stress ages on inflammation related genes [24-25].
related disorders through the psychosocial effects In the presence of norepinephrine there is an
of halitosis, poor oral hygiene and edentulism. increase in transcriptional activity on genes that
These could impact the patient’s quality of life by are related to the production of interleukin 1
inducing shame, social isolation and depression (IL1), tumor necrosis factor (TNF) and IL6 [26] with
[17-18]. Alongside periodontitis putative effects on systemic pro-inflammatory effects. The role of the
depression, there is significant longstanding evi- above mentioned cytokines in periodontitis has
dence that it imposes a greater risk on systemic been studied and reviews concluded on their pro-
conditions such as cardiovascular disease or preterm inflammatory role and bone resorption activity
delivery [19]. in the presence of an infection [27]. Focusing on
However, the link between periodontal disease and the periodontium, the catecholamine secretion in
other systemic conditions seems to be bidirectional, response to these stressful stimuli, as proposed on the
as it is well documented that diabetes and osteo- SNS pathway, can have an influence on proteolytic
porosis increase the risk for periodontitis [20]. enzymes with a tissue destructive potential, such as
Analyzing these links, a common denominator has matrix metalloproteinases MMP [28].
caught the attention of researchers. Considering the
well-accepted fact that stress is related to cardio- 3.5. Hypothalamic-pituitary-adrenal axis
vascular disease, diabetes mellitus, preterm A stressful stimuli of a less acute type is perceived
delivery, osteoporosis, rheumatoid arthritis, infla- by the brain and signals the hypothalamic/pituitary/
mmatory bowel disease, and systemic lupus erythe- adrenal (HPA) axis to release corticotropic-releasing
matosus through physiological or behavioral hormone (CRH) from the hypothalamus which
responses, this could point to stress as a common risk induces the release of adrenocorticorticotropic
indicator for these conditions and periodontitis [9]. hormone (ACTH) from the pituitary gland and
consecutively glucocorticoids from the adrenal
3.3. Pathophysiology of stress- biological mechanisms cortex [29]. Glucocorticoids suppress the immune
Stress is one of the adaptive mechanisms that system functions by a number of mechanisms. They
helps individuals navigate through challenges of all decrease the number of circulating lymphocytes,
natures, making it compatible with survival forms monocytes, and eosinophils; inhibit the functions of
of organisms. However, when there is a mismatch inflammatory cells through a myriad of actions such

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as lowering the production of cytokines (interleukin between stress-driven behavioral changes and perio-
Review Articles [IL] IL-1, IL-2, IL-3, IL-6, tumor necrosis factor (TNF), dontal conditions, as presented below. It is now
interferon gamma. The cascade of the inflammation is widely accepted that one of the mechanism through
further hindered due to an impeding of macrophage- which stress is thought to exert its putative effect on
antigen presentation and lack of lymphocyte the periodontal condition is the behavioral change
differentiation into more specialized cells such as in general, with stressful individuals inclined towards
T-helper lymphocytes, B cells, cytotoxic lymphocytes adopting harmful health behaviors including oral
and NK cells [30]. Glucocorticoids can further suppress hygiene neglecting, smoking and poor compliance
the immune responses by impeding the functions of with dental care [9]. In a study conducted by Deinzer
secretory IgA and IgG, and neutrophils all of which et al. [37] assessing the effect of academic stress
are important factors that build the host response on gingival inflammation, the crevicular levels of
towards infections by pathogenic bacteria. Under this interleukin-beta were higher and the oral hygiene
altered defense response, periodontal infection levels were poorer compared to the control group,
can occur which may lead to tissue destruction by indicating that academic stress was a risk factor for
factors such as IL-1 and MMP and the direct effects gingivitis. Emotional conditions that generate higher
of pathogenic periodontal microorganisms [9]. There stress levels are also thought to affect the choice of
is yet another mechanism that could be involved in a diet with an inclination towards softer foods with
elevated levels of inflammation that are related to a high content of sugars and fat which facilitate the
HPA-axis response to stress. faster formation of plaque and enhance its adhering
capacity to the teeth, affecting the periodontal health
3.6. Increased inflammation via glucocorticoid resist- [38]. During periods of elevated stress individuals
ance - HPA-axis related tend to increase smoking or even start it as a new
When a persistent secretion of glucocorticoids occurs, habit. The harmful effects of smoking on oral health
immune cells in response lower their sensitivity to it, and particularly that of the periodontium, are well
developing what is known as glucocorticoid studied and established beyond doubts [39].
resistance [31]. In response to this phenomenon,
HPA axis that is responsible for providing the “fight 5. CONCLUSIONS
or flight” reaction to threatening stimuli of a social-
environmental nature, can mount an abnormally high The present body of knowledge emerging from
inflammatory response, when triggered frequently or periodontology and psychoneuroimmunology inter-
chronically. Under conditions of prolonged actual or disciplinary field has yielded strong evidence on the
perceived threat, or possibly during acute stressors relation of stress and periodontitis.
indicating social threat or physical danger, gluco- The intriguing evidence of the effects of stress on the
corticoid resistance can develop, leading to excessive inflammatory conditions and periodontitis should
inflammation that increases a person’s risk for several guide researchers to explore its implications on the
disorders [23]. A few other disorders such as anxiety, possible preventive measures, as well as treatment
posttraumatic stress disorder, asthma, rheumatoid modalities.
arthritis, cardiovascular disease, inflammatory bowel Informed clinicians can then make better informed
disease, autoimmune diseases, and some cancers, decisions and design treatment plans on patients
also show evidence of glucocorticoid resistance that might include addressing psychological
[32-34]. This, together with the growing body of disturbances and referring them to specialists for an
evidence that periodontal disease is linked to integrated care plan.
the abovementioned conditions through several In a multifactorial disease such as periodontitis,
physiopathological processes, might suggest that there is a necessity for multidisciplinary attention
glucocorticoid insensitivity happening under and collaboration in considering the psycho-
stressful environmental stimuli could be involved in logical status of the individual along other well-
the progression of periodontitis. Another pathway established etiological factors.
by which stress induced physiologic response This approach would yield multiple benefits for the
modulates the immune system is the sensonic patient, with general health to be seen as a good
peptidergic nervous pathway, also known as balance between body and mind.
“neurogenic inflammation” in which neuropeptides
are released from sensory nerve fibers while CONFLICT OF INTEREST
stimulated by external stimuli [35 -36]. Research has Authors declare no conflict of interest related to this manuscript.
provided evidence that the peripheral release of
neuropeptides may promote various inflammatory AUTHORS CONTRIBUTION
processes [36].
OM: Data gathering, Data analysis, Data Interpretation,
Manuscript drafting, RB: Data interpretation, Manu-
4. DISCUSSION script revision, BR: Data gathering, Data analysis.
Literature contains various studies conducted
on humans aiming at evaluating the association

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Review Articles
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Oriola MADHI
DDS, PhD Student, Clinical Professor
Department of Periodontology and Conservative Dentistry
Faculty of Dental Medicine
University of Medical Sciences
Tirana, Albania

CV
Oriola Madhi studied dentistry at the Faculty of Dental Medicine, University of Medical Sciences in Tirana, Albania where
she earned her DDS degree. Afterwards she was accepted into a residency program in Dental Therapy in the same faculty.
She went on to advance her academic education by enrolling into a PhD program in the field of Periodontology and is close
to the completion of the program. She has been teaching at the Faculty of Dental Medicine for 8 years and she is also a
practicing dentist and clinical instructor at the University Dental Clinic. Her teaching areas include conservative dentistry and
periodontology.

Questions
1. The advanced forms of periodontitis affect?
qa. Over 50% of the world population;
qb. More individuals than the milder forms of periodontitis;
qc. Less than 15% of the world population;
qd. Only immunocompromised patients.

2. In a study exploring the effect of stress on NUG, by measuring the corticosteroid levels
in the patient’s urine, NUG patients compared to the control group exhibited?
qa. Lower levels of corticosteroids in their urine;
qb. Higher levels of corticosteroid in their urine;
qc. Same levels of corticosteroid in their urine;
qd. No statistical difference between groups.

3. Glucocorticoids, suppress the immune system functions by?
qa. Inhibiting the functions of inflammatory cells;
qb. Increasing the production of cytokines;
qc. Increasing the production of secretory IgA and IgG;
qd. Increasing the number of NK cells.

4. In a study exploring the effects of academic stress on gingival inflammation, it was
observed?
qa. An increase in the crevicular levels of interleukin β;
qb. A decrease in the crevicular levels of interleukin β
qc. An improvement on oral hygiene;
qd. No difference on inflammation markers between groups.

122 Stoma Edu J. 2020;7(2): 117-122 pISSN 2360-2406; eISSN 2502-0285