Literature Review/Sports Dentistry
Overreaching: a risk factor for periodontal disease?
Bárbara Capitanio de Souza1
1Brazilian Academy for Sports Dentistry, Rio de Janeiro, RJ, Brazil
• Conflicts of interest: none declared.
Objective: to identify the effects of overreaching on the susceptibility to develop periodontal diseases. Material and Methods: search for scientific articles on the Pubmed database. The search strategy used the term “overreaching” with the Boolean operator “and”, and the keywords: effects, immunological, diagnosis. The descriptor “periodontal disease and risk factor” was also used. The studies selected were analyzed and the studies that did not cover the proposed subject were excluded. Results: periodontal diseases involve a multi-factorial etiology. Although the presence of microbiological pathogens is an important factor for the devel-opment of the diseases, other factors have also been highly correlated with their prevalence. The dysfunction of the immune function is more pronounced when the exercise is continuous, prolonged and moderately intense, condition that occurs in overreaching. There is a possibility that the combined effects of changes in immu-nological parameters may compromise the response to some diseases, such as periodontal diseases. The destruction of the periodontal tissues is a final consequence of the immune response from the host, which can vary in overreaching. Conclusion: overreaching may be responsible for alterations in the immune system of the athlete. Diseases that present a common inflammatory profile may suffer additional modulations because of this process, leaving these individuals under a higher risk. Keywords: Oral health; Physical education and training; Periodontal diseases.
Periodontal diseases are infectious and inflammatory
diseases that affect hard and soft tissues around the
teeth.1 They are characterized by the destruction of
the connective tissue and periodontal bone support after an inflammatory response from the host, secondary to the
bacterial infection.2 The microbial challenge can lead to an
imbalance in the disease process, modifying the size and severity of the immunoinflammatory response, which may also be modulated by environmental, genetic and individual
Periodontal diseases have effects beyond the ones on the oral tissues and they have been linked to a condition of systemic inflammation, resulting in increased risk of sub-sequent chronic diseases such as cardiovascular diseases, diabetes mellitus, low birth weight infants, rheumatoid
arthritis, metabolic syndrome, and nowadays, cancer.5
Al-though this relation has been reported in many
publica-tions, the nature of such a link is still little understood.6 On
the other hand, periodontal diseases involve multi-factorial etiology. Although the presence of microbiological patho-gens is an important factor for the development of diseases, lifestyle factors such as smoking, diet and oral hygiene have also been highly correlated with the prevalence of periodon-titis.7
Periodontal diseases are infectious and inflammatory, and as such, they are subject to modulations of the immune system. Currently, the idea that the susceptibility to these diseases may be associated with different factors is widely accepted, which is emphasized by the fact that some people
are more prone to periodontal diseases.8 The changes that
can occur in the immune response are partially responsi-ble for impact on the susceptibility and severity of the
dis-ease, a better understanding of this relation can contribute to the understanding of the pathogenesis of the periodontal disease and on the control of risk factors in individuals of
Athletes who make great efforts to achieve performance levels within their modality seem to present high prevalence
of oral diseases.9 This condition may be associated to
chang-es of parameters of the immune system, arising from the intense practice of sports. The increase in the intensity and amount of training are undertaken by athletes to improve their physical performance. However, when the balance between the appropriate training stress and adequate re-covery is interrupted, acute fatigue may result in a negative response to performance, which can be followed by
over-compensation, known as functional overreaching (F-OR).10
The prolonging of a state of low performance associated to other stress factors increases the loss of performance and prolongs the recovery state, also involving an inadequate response to the excessive exercise that could result in dif-ferent physiological disturbances, known as non-functional overreaching (NF-OR). The evolution of this condition can affect the neurological, immune, and endocrine functioning of an athlete and is related to the development of
overtrain-ing syndrome (OTS).11
Prolonged episodes of strenuous exercise cause a tempo-rary depression of various aspects of the immune function. The dysfunction of the immune function after exercising is more pronounced when the exercise is continuous, pro-longed, of moderate to high intensity and without proper
diet.12 Thus, it is possible that the combined effects of
chang-es in immunological parameters can compromise rchang-esponse to some diseases, such as in the periodontal diseases. There-fore, understanding the etiological factors and the
patho-genesis of the periodontal disease is important to better un-derstand the associated risk factors. Thus, the objective of this study was to identify the effects of overreaching on the susceptibility to develop periodontal diseases.
Material and Methods
A search for scientific articles on the Pubmed database was performed to achieve this objective. The search strate-gy used the term “overreaching” with the Boolean operator “and”, and the keywords: effects, immunological, diagnosis. The descriptor “periodontal disease and risk factor” was also used. The studies selected were analyzed and the studies that did not cover the proposed subject were excluded (Figure 1).
Modifiable Risk Factors for Periodontal Diseases
Risk factors are particularities of individuals that may put them at greater risk of contracting a disease. They are considered as characteristics, behavior or exposure with an association to a certain disease; however, this relation is not necessarily of causal nature since it does not directly
determines the onset or the progression of the disease.13 To
be considered as a risk factor for periodontal diseases, the factor must be associated with the disease and responsible for the development of an adaptive immune response on the body and its elimination or suppression should result in the
remission of the condition.14 By analyzing the criteria
men-tioned in literature, we noted that periodontal diseases have
risk factors reported as systemic and local to be considered.15
Modifiable risk factors include characteristics of the local microbiota, quality of the oral biofilm, presence of plaque retention factors, dental calculus, dental restorations and
occlusal and anatomical factors.14 The oral microbiota is
the most explored factor in studies involving the
etiopatho-genesis of periodontal diseases among the ones presented; however, although the presence of pathogenic microorgan-isms is a factor that causes this condition, it is not enough to
cause periodontal diseases.5 The oral microbiota contributes
to the development of periodontal diseases by interfering in the microbial homeostasis of the host, and not because of
simple development of a few pathogens.16
Susceptibility to periodontal diseases and other inflam-matory diseases seems to change in response to interac-tions of risk factors during the lives of individuals. Many modifiable systemic risk factors contribute to the increase in systemic inflammatory markers and modify the
genet-ic regulation through a variety of biologgenet-ical mechanisms.17
Periodontal diseases are related to common modifiable risk factors, such as smoking, stress and depression, alcohol, obesity, diabetes, metabolic syndrome, osteoporosis,
behav-ioral factors, among others.18 Currently, there is significant
evidence that smoking and diabetes are major factors not only to the development of periodontal diseases, but also to
the severity and progression of diseases.15, 19 The
inflamma-tory profile common to the conditions seems to be the main factor of synergism, being responsible for the overlap of the
Non-Modifiable Risk Factors for Periodontal Diseases
Non-modifiable risk factors, such as age, sex and ethnic-ity are involved in the prevalence and severethnic-ity of
periodon-tal disease.20 Periodontal diseases are not universal because
there is a variation of existence and severity within the population that presents susceptibility. The risk of illness is dynamic and changes in response to complex interactions
of different characteristics.13 Understanding the risk factors
is essential for clinical practice; therefore, identifying these factors helps guiding the patients for the prevention and
Literature points the age of the individual as an important factor in the prevalence and severity of periodontal diseases. Adults present a higher prevalence of the disease when com-pared to younger populations; however, there is no definitive response to this relation, if there is an individual effect on the existence of periodontal diseases or it is a consequence
of the cumulative characteristics of the disease.20 When we
consider the sex factor, we observed a greater distribution of the disease among men in relation to women. The reasons for this difference between sexes is not well explained, but it can be attributed to hygiene care and other habits such as
smoking.21 When the prevalence of periodontal diseases is
assessed in relation to different ethnic groups a discrepan-cy among different results is observed, creating a difficulty to establish a causal relationship between the factors with certainty. There is possibility of genetic variations affecting this correlation. Additionally, other risk factors may affect
periodontal diseases among populations.17,22
Additionally, some authors also point to other risk factors for periodontal diseases, such as socioeconomic status,
ed-ucational level and genetic factors.2,17 Data from the studies
indicate that the socioeconomic status and the educational level seem to relate to the presence of periodontal diseas-es; periodontal tissues from people in higher economic and
educational levels present better health.2,23 Current studies
have shown an increased risk of periodontal diseases with variations in the genes related to inflammatory response. A study indicates that genetic polymorphisms of inflammato-ry factors may influence the development or progression of
periodontal diseases.24 Furthermore, genetic risk factors are
associated with the presence and severity of the disease, as the risk of periodontal diseases seems to be consistent with elements of heritable susceptibility.
The increase in the intensity and amount of training is usually performed to enhance physical performance. The intensified training may result in a decline in perfor-mance; however, if adequate recovery periods are provided, an effect of overcompensation may occur, resulting in an improvement in performance when compared to the initial
values.10-12 Based on the principles of sports training, F-OR
can be understood as the accumulation of training stress and other factors that result in a temporary decrease of the performance levels. This state of low performance levels can last from a few days to two weeks and a process of
overcom-pensation occurs after this.10 The mechanisms that involve
the emergence of overreaching are diverse and depend on the relation between training and an adequate recovery period, besides the existence or control of other additional
stress factors.25, 26
F-OR is often intentionally promoted by periods of in-tense training with the objective of stimulating a tempo-rary decrease of performance levels followed by an induced overcompensation of performance. However, evidences sup-porting a maximized training response after F-OR are not
fully clarified yet.27 Lack of appropriate control of the F-OR
stage may result in a stagnation or decline in performance, increasing the duration of the physical recovery period and inducing NF-OR. Additionally, biochemical, immunolog-ical and physiologimmunolog-ical alterations may be presented by the athlete, with the possibility of developing other health
The development of NF-OR is related to the persistence of the period of intense training. Increased levels of per-formance drop associated to psychological and hormonal disorders, mood changes, weight loss and sleep disorders
can be observed in this condition, and the recovery may
happen within a few weeks or months.10 The effectiveness
of the physical training depends on physiological factors and parameters of the athletes, on the workload and on the individual susceptibility to tolerate fatigue. Depending on the workload applied, different responses to training can be
induced.28 The excessive physical stress imposed by training
can result in an inflammation powerful enough to induce subsequent responses, such as those involving the catabolic processes.
Infections and respiratory diseases are complaints that affect the athletes, and the occurrence of these diseases is particularly high during periods of intense training or competition. Exercise triggers the simultaneous increase of antagonistic inflammatory mediators. Disorders in the production profile of cytokines and defense cells may oc-cur as a response to NF-OR, increasing the susceptibility
to an infection.11 The intensity and the amount of training
during NF-OR may be responsible for changes in the im-mune function, such as the change in the phagocytic activ-ity of defense cells, reduced production of immunoglobulin
A and increased oxidative stress.29 The NF-OR state can lead
to OTS which presents more diffuse characteristics, nega-tively affecting multiple systems and having a much slower recovery process.
OTS can be characterized as a neuroendocrine disorder that occurs in the hypothalamic-pituitary axis due to the imbalance between the intensity of the exercise performed and the responsiveness of the system. Significant reduction of physical performance accompanied by very important physiological, psychological and biochemical changes
oc-cur during this condition.11 OTS can also be associated to
situations of systemic inflammation and subsequent effects on the central nervous system, including mood swings and central fatigue. The recovery of the athlete in OTS is slower
and can take weeks or months.10
OTS can be classified into two categories. The sympa-thetic form is characterized by the increase in activity of the sympathetic nervous system, which causes basic chang-es of the body functions and facilitatchang-es the motor rchang-esponse to acute stress or physical activity. It can be influenced by the emotional state of the athlete and by factors not related to training. The parasympathetic form is characterized by the predominance of the parasympathetic tone during rest and exercise, and it is observed more frequently in
endur-ance athletes.30-32 The capacity of adaptation, physiological
characteristics, the volume of the intense training and the total amount of internal and external stress factors will de-termine the greater vulnerability of some athletes to
8. Van Dyke TE. Cellular and molecular susceptibility determinants for peri-odontitis. Periodontol 2000. 2007;45:10-3.
9. Ashley P, Di Iorio A, Cole E, Tanday A, Needleman I. Oral health of elite ath-letes and association with performance: a systematic review. Br J Sports Med. 2015;49(1):14-9.
10. Aubry A, Hausswirth C, Louis J, Coutts AJ, Buchheit M, Le Meur Y. The De-velopment of Functional Overreaching Is Associated with a Faster Heart Rate Recovery in Endurance Athletes. PLoS One. 2015;10(10):e0139754.
11. Jeffrey B Kreher. Diagnosis and prevention of overtraining syndrome: an opinion on education strategies. Open Access J Sports Med. 2016;7:115-22. 12. Halson SL. Monitoring training load to understand fatigue in athletes. Sports Med. 2014;44(Suppl 2):S139-S1347.
13. Reynolds MA. Modifiable risk factors in periodontitis: at the intersection of aging and disease. Periodontol 2000. 2014;64(1):7-19.
14. Kornman K. The Pathogenesis Paradigm. J Periodontol. 2008;79:1560-8. 15. Ronderos M, Ryder MI. Systemic Disease Overview-Risk Assessment in Clin-ical Practice. Periodontol 2000. 2004;34:120-35.
1. Liu KZ, Xiang XM, Man A, Sowa MG, Cholakis N, Ghiabi E, et al. In vivo determination of multiple indices of periodontal inflammation by optical spec-troscopy. J Periodontal Res. 2009;44(1):117-24.
2. Yousef A. Risk Factors of Periodontal Disease: Review of the Literature. Int J Dent. 2014; 2014:182513. doi:10.1155/2014/182513.
3. Liu L, Li C, Cai C, Xiang J, Cao Z. Cyclophilin A (CypA) is associated with the inflammatory infiltration and alveolar bone destruction in an experimental periodontitis. Biochem Biophys Res Commun. 2010;391(1):1000-6.
4. Ebersole JL, Steffen MJ, Reynolds MA, Branch-Mays GL, Dawson DR, Novak KF, et al. Differential Gender Effects of a Reduced Calorie. J Periodontal Res. 2008;43(5):500-7.
5. Lindroth AM, Park YJ. Epigenetic biomarkers: a step forward for understand-ing periodontitis. J Periodontal Implant Sci. 2013;43(3):111-20.
6. Mawardi HH, Elbadawi LS, Sonis ST. Current understanding of the relation-ship between periodontal and systemic diseases. Saudi Med J. 2015;36(2):150-8. 7. Van der Velden U, Abbas F, Armand S, Loos BG, Timmerman MF, Van der Weijden GA, et al. Java project on periodontal diseases. The natural development of periodontitis: risk factors, risk predictors and risk determinants. J Clin
Overreaching as a Risk Factor for Periodontal Diseases
Periodontal diseases are common oral diseases world-wide and are an important public health concern because of the substantial treatment cost. They are characterized by the inflammation and destruction of the tissues of teeth
sup-port, being the main cause of tooth loss.33 Periodontal
dis-eases present infectious and inflammatory characteristics, as they are subject to the variations and modulations of the immune system as well as conditions that can modify the response of the defense of the body. The immune response plays an important role in the pathogenesis of various dis-eases and their systemic complications, in addition to
spe-cific functions during physiologic conditions.34 Despite its
infectious etiology, the destruction of periodontal tissues is
a consequence end of the immune response of the host.33
Different physiologic conditions can modulate the degree of systemic immune response by controlling the produc-tion profile of defense cells and immunological mediators, who work at the interface of inflammatory processes, such
as those that occur in periodontal diseases.5 The regulation
of the expression of enzymes and proteins that act on peri-odontal inflammatory response is well established, as well as the stimulation, migration and stoppage of immune cells, exacerbation and resolution of the inflammatory responses by complement processing, cytokines and other bioactive
molecules.33 Exercise can have positive and negative effects
on immune function and susceptibility to diseases. Physi-cal activity of moderate to high intensity can cause immune changes, being responsible for a transient immunodepres-sion commonly observed after acute and chronic or
Both the number and the functional capacity of the de-fense cells can be lessened by repeated episodes of intense exercise, such as during NF-OR. The reason probably is re-lated to increased levels of stress hormones during exercise.
Additionally, the concentration of glutamine is important for the function of certain cells of the immune system, it has also been suggested as a possible cause of
immunode-pression associated to intense training.36 Also, during
exer-cise, an increase in the production of reactive oxygen species can happen and some cellular functions can be impaired by an excess of free radicals. Reduced levels of immunoglob-ulin and salivary antimicrobial proteins can also be found
Immune cell functions are temporarily impaired follow-ing acute episodes of intense or continuous exercise, and athletes involved in this type of training seem to be more susceptible to infections; in addition, there seems to be a dif-ference in the prevalence of these diseases in athletes, taking
more time for recovery.10 This is important for the athlete
patient, because even minor infections can result in drops of exercise performance and capability to sustain the inten-sity of practices. The physiological conditions that involve overreaching feature a median temporal characteristic, and sometimes it limits the natural evolution of some diseases. However, the high prevalence of periodontal diseases in this population must be considered; an episode of major evolu-tion of diseases and risk of acute condievolu-tions related to peri-odontal diseases can occur under these conditions.
The physiological condition caused by the physical stress from intense training, such as those involving overreaching, may be responsible for changes in the immune system of an athlete. In these situations, diseases that present a common inflammatory profile may suffer additional modulations because of this process, leaving these individuals under a higher risk. Considering this biological plausibility between the two conditions as possible, further research for the clar-ification of this relation is important, since there is little lit-erature about it.
16. Hajishengallis G, Lambris JD. Complement and dysbiosis in periodontal dis-ease. Immunobiology. 2012;217:1111-6.
17. Genco RJ, Borgnakke WS. Risk factors for periodontal disease. Periodontol 2000. 2013;62(1):59-94.
18. Jansson H. Studies on periodontitis and analyses of individuals at risk for periodontal diseases. Swed Dent J Suppl. 2006;(180):5-49.
19. Johannsen A, Susin C, Gustafsson A. Smoking and inflammation: evidence for a synergistic role in chronic disease. Periodontol 2000. 2014;64(1):111-26. 20. Oppermann RV. An overview of the epidemiology of periodontal diseases in Latin America. Braz. Oral Res. 2007;21:8-15.
21. Meisel P, Reifenberger J, Haase R, Nauck M, Bandt C, Kocher T. Women are periodontally healthier thanmen, but why don’t they have more teeth than men? Menopause. 2008:15(2):270-5.
22. Beck JD, Koch GG, Rozier RG, Tudor GE. Prevalence and risk indicators for periodontal attachment loss in a population of older community-dwelling blacks and whites. Journal of Periodontology. 1990;61(8):521-8.
23. Gilbert GH. Racial and socioeconomic disparities in health from popula-tion-based research to practice-based research: the example of oral health. J Dent Educ. 2005;69(9):1003-14.
24. Ari G, Cherukuri S, Namasivayam A. Epigenetics and Periodontitis: A con-temporary review. J Clin Diagn Res. 2016;10(11):ZE07-ZE09.
25. Smith LL. Cytokine hypothesis of overtraining: a physiological adaptation to excessive stress? Med.Sci. Sports Exerc. 2000;32:317-31.
26. Meeusen R, Duclos M, Gleeson M, Rietjens G, Steinacker J, Urhausen A. Pre-vention, diagnosis and treatment of the overtraining syndrome. Eur J Spo Sci. 2006;6:1-14.
27. Meeusen R, Duclos M, Foster C, Fry A, Gleeson M, Nieman D, et al. European College of Sport Science, Americam College of Sports Medicine. Prevention,
di-agnosis, and treatment of the overtraining syndrome: joint consensus statement of the European College of Sport Science and the American College of Sports Medicine. Medicine and science in sports and exercise. 2013;45(1):186-205. 28. Hiscock N, Pedersen BK. Exercise-induced immunodepression – Plasma glu-tamine is not the link. J Appl Physiol. 2002;93:813-22.
29. Lee N, Kim J, Hyung GA, Park JH, Kim SJ, Kim HB, et al. Training Effects on Immune Function in Judoists. Asian J Sports Med. 2015;6(3):e24050.
30. Konig D, Wagner KH, Elmadfa I, Berg A. Exercise and oxidative stress: sig-nificance of antioxidants with reference to inflammatory, muscular, and systemic stress. Exerc Immunol Ver. 2001;7:108-33.
31. Mackinnon LT. Overtraining effects on immunity and performance in ath-letes. Immunol Cell Biol. 2000;78:502-9.
32. Petibois C, Cazola G, Poortmans JB, Deleris G. Biochemical aspects of over-training in endurance sports: a review. Sports Med. 2002;32(13):867-78. 33. Franco C, Patricia HR, Timo S, Claudia B, Marcela H. Matrix metalloprotein-ases as regulators of periodontal inflammation. Int J Mol Sci. 2017;18(2):pii:E440. 34. Heron SE, Elahi S. HIV infection and compromised mucosal immunity: oral manifestation and systemic inflammation. Front Immunol. 2017;8:241. doi: 10.3389/fimmu.2017.00241.
35. Ziemann E, Zembroñ-Lacny A, Kasperska A, Antosiewicz J, Grzywacz T, Garsztka T, et al. Exercise training - induced changes in inflammatory mediators and heat shockproteins in young tennis players. J Sports Sci Med. 2013;12(2):282-9. 36. Svendsen IS, Killer SC, Carter JM, Randell RK, Jeukendrup AE, Gleeson M. Impact of intensified training and carbohydrate supplementation on immuni-ty and markers of overreaching in highly trained cyclists. Eur J Appl Physiol. 2016;116(5):867-77.
37. Papacosta E, Nassis GP. Saliva as a tool for monitoring steroid, peptide and im-mune markers in sport and exercise science. J Sci Med Sport. 2011;14(5):424-34.
Submitted: 07/27/2017 / Accepted for publication: 10/31/2017 Corresponding Author
Bárbara Capitanio de Souza E-mail: email@example.com
1. Bárbara Capitanio de Souza – DDS and MSc. SOUZA BC