Pathophysiology mechanisms of the stress impact on periodontal tissues

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Pathophysiology mechanisms of the stress impact on periodontal tissues

Denefil O.V. Denefil Olha Volodymyrivna DMS, professor, Pathological Physiology Department, I. Horbachevsky Ternopil National Medical University, Ternopil, Chorniy S.V. Chorniy Sofiia Volodymyrivna student of I.Horbachevsky Ternopil National Medical University, Ternopil, Boitsaniuk S.I. Boitsaniuk Svitlana Ivanivna PhD, associate professor, Department of Dental Therapy, Dean of Dentistry Faculty, I.Horbachevsky Ternopil National Medical University, Ternopil, Manashchuk N.V. Manashchuk Nadia Volodymyrivna PhD, associate professor, Department of Dental Therapy, Faculty of Dentistry, I.Horbachevsky Ternopil National Medical University, Ternopil,

Pohoretska K.V. Pohoretska Khrystyna Vasylivna PhD, associate professor, Department of Dental Therapy, Faculty of Dentistry, I.Horbachevsky Ternopil National

Medical University, Ternopil, Chornij N.V. Chornij Natalia Volodymyrivna PhD, associate professor, Department of Dental Therapy, Faculty of Dentistry, I.Horbachevsky Ternopil National

Medical University, Ternopil, Levkiv M.O. Levkiv Mariana Orestivna PhD, associate professor, Department of Dental Therapy, Faculty of Dentistry, I.Horbachevsky Ternopil National Medical University, Ternopil, Patskan L.O. Patskan Liudmyla Oleksandrivna PhD, associate professor, Department of Dental Therapy, Faculty of Dentistry, I.Horbachevsky Ternopil National Medical University, Ternopil,

Patskan L.O. Gryniuka Iurii Romanovych member of UAP (Ukrainian Academy of Periodontology), dentist - surgeon of dental clinic "Studio of Periodontology"

Ternopil



Abstract

Stresses of wartime: chronic long-term and acute short-term stress episodes that periodically increase it, can be physiological and neuropsychological (psycho-emotional). Constant fatigue, anxiety and long-term stress exhaust the body, harm the physical condition, can become a trigger for depression, the development of post-traumatic stress disorder, and this, in turn, can cause the development of pathological conditions of organs and systems, in particular periodontal tissues. Purpose of the article is to review available in free access scientific papers on the problem of pathophysiological mechanisms of the influence of stress on periodontal tissues, emphasizing the emerging role of neuroendocrine and neuroimmune mediators in the pathophysiology of inflammatory diseases.

Materials and methods. Relevant literature from MEDLINE (PubMed), Google Scholar, and in open access journals which are published by Elsevier was selected using the following key words «adrenal glands», «cortisol», «endocrine system», «periodontal disease», «stress» were used in various combinations. The search considered works published from 2010 until November 2023 by using the abovementioned key words as we want to include only up to date information. In total there were found 202 scientific papers corresponding to above mentioned key words. To the selected scientific papers we applied the inclusion and exclusion criteria to choose the relevant ones.

Results. A comprehensive study of the available information related to relationship between psychological disturbances and periodontal disease was carried out. Stress triggers emotional and physiological responses and serves as a significant modifiable risk factor for both mental and physical health conditions. Wars have profound social, economic, and psychological consequences for affected individuals and communities. The initiation and progression of periodontitis are related to multiple aetiologic and risk factors, the most important of which are the local microbiota and host immune response. It is established that stress reduces the flow of salivary secretions which in turn can enhance dental plaque formation. The depressed individuals have been shown to possess a higher concentration of cortisol in gingival crevicular fluid, and they respond poorly to periodontal treatment. Conclusion. In summary, chronic stress negatively impacts periodontal health, highlighting the importance of addressing stress as part of overall well-being. Therefore, the study of the impact of stress on the development and course of periodontal diseases and the further development of appropriate schemes of prevention and rational pharmacotherapy is a promising and urgent task of today's dentistry.

Keywords: adrenal glands, cortisol, endocrine system, periodontal disease, stress.



Анотація

Патофізіологічні механізми впливу стресу на тканини пародонта

Денефіль Ольга Володимирівна доктор медичних наук, професор кафедри патологічної фізіології, Тернопільський національний медичний університет імені І. Я. Горбачевського МОЗ України, м. Тернопіль

Чорній Софія Володимирівна студентка, Тернопільський національний медичний університет імені І.Я. Горбачевського МОЗ України, м. Тернопіль

Бойцанюк Світлана Іванівна кандидат медичних наук, доцент кафедри терапевтичної стоматології, декан стоматологічного факультету, Тернопільський національний медичний університет імені І. Я. Горбачевського МОЗ України, м. Тернопіль

Манащук Надія Володимирівна кандидат медичних наук, доцент кафедри терапевтичної стоматології, Тернопільський національний медичний університет імені І.Я. Горбачевського МОЗ України, м. Тернопіль

Погорецька Христина Василівна кандидат медичних наук, доцент кафедри терапевтичної стоматології, Тернопільський національний медичний університет імені І. Я. Горбачевського МОЗ України, м. Тернопіль

Чорній Наталія Володимирівна кандидат медичних наук, доцент кафедри терапевтичної стоматології, Тернопільський національний медичний університет імені І.Я. Горбачевського МОЗ України, м. Тернопіль

Левків Мар'яна Орестівна кандидат медичних наук, доцент кафедри терапевтичної стоматології, Тернопільський національний медичний університет імені І.Я. Горбачевського МОЗ України, м. Тернопіль

Пацкань Людмила Олександрівна кандидат медичних наук, доцент кафедри терапевтичної стоматології, Тернопільський національний медичний університет імені І.Я. Горбачевського МОЗ України, м. Тернопіль

Гринюка Юрій Романович член УАП (Української академії пародонтології), лікар стоматолог-хірург стоматологічної клініки «Студія пародонтології», м. Тернопіль

Стреси воєнного часу: хронічні довготривалі та гострі короткочасні стресові епізоди, які періодично посилюють його, можуть бути фізіологічними та нервово-психічними (психоемоційними). Постійна втома, хвилювання та тривалий стрес виснажують організм, шкодять фізичному стану, можуть стати поштовхом до депресії, розвитку посттравматичного стресового розладу, а це, у свою чергу, може спричинити розвиток патологічних станів органів та систем, зокрема тканин пародонту.

Метою статті є огляд наявних у вільному доступі наукових праць з проблеми патофізіологічних механізмів впливу стресу на тканини пародонту, підкреслюючи зростаючу роль нейроендокринних та нейроімунних медіаторів у патофізіології запальних захворювань.

Матеріали та методи. Відповідну літературу з MEDLINE (PubMed), Google Scholar та журналів у відкритому доступі, які видає Elsevier, було відібрано за такими ключовими словами «надниркові залози», «кортизол», «ендокринна система», «хвороби пародонту», «стрес» використовувалися в різних поєднаннях. Пошук враховував роботи, опубліковані з 2010 року до листопада 2023 року, з використанням вищезазначених ключових слів, оскільки ми хотіли включити лише актуальну інформацію. Всього було знайдено 202 наукові праці, які відповідали вищезазначеним ключовим словам. До вибраних наукових робіт ми застосували критерії включення та виключення, щоб вибрати відповідні.

Результати. Проведено комплексне вивчення наявної інформації про взаємозв'язок психічних розладів із захворюваннями пародонту. Стрес викликає емоційні та фізіологічні реакції та є значним модифікованим фактором ризику як для психічного, так і для фізичного здоров'я. Війни мають глибокі соціальні, економічні та психологічні наслідки для постраждалих людей. Початок і прогресування генералізованого пародонтиту пов'язані з кількома етіологічними факторами та факторами ризику, найважливішими з яких є мікроорганізми та імунна відповідь організму. Встановлено, що стрес зменшує виділення слини, що, у свою чергу, може посилити утворення зубного нальоту. Було показано, що у людей з депресією концентрація кортизолу в рідині ясенної борозни вище, і вони погано реагують на лікування захворювань пародонту.

Висновок. Загалом, хронічний стрес негативно впливає на здоров'я тканин пародонту, підкреслюючи важливість вирішення проблеми стресу як частини загального благополуччя. Тому вивчення впливу стресу на розвиток і перебіг захворювань пародонту та подальша розробка відповідних схем профілактики та раціональної фармакотерапії є перспективним і актуальним завданням сучасної стоматології.

Ключові слова: надниркові залози, кортизол, ендокринна система, пародонтоз, стрес.



Abstract

Formulation of the problem. The war in Ukraine and the events related to it, affect many people. Every day lived by Ukrainians is filled with informational stress factors for them [1]. Stress applies to everyone: military personnel, residents of occupied regions, displaced persons and refugees, as well as those who are lucky enough to live in relatively peaceful areas [2]. Nowadays, stress is present in the life of every person. However, its strength, intensity, and mental and physical health consequences can differ. Constant overwork, anxiety, and long-term stress exhaust the body, harm the physical condition, and can become a trigger for depression and the development of post-traumatic stress disorder. The situation described above, in turn, can cause pathological conditions of organs and systems in particular periodontal tissues.

Analysis of the latest research and publications. High prevalence of periodontal disease in adult population makes it a public health concern. Periodontal disease, in its strictest sense, encompasses both gingivitis and periodontitis. It is triggered by microbial plaque but affects only a subset of the population. Periodontitis explicitly destroys the supporting structures around teeth, including the periodontal ligament, bone, and soft tissues. Notably, periodontitis is the most significant of these diseases because it leads to tooth loss. While the etiology of periodontitis remains incompletely understood, it is likely the result of an opportunistic infection.

Factors such as an increase in the number of pathogenic plaque microorganisms, their ability to invade tissue, and the individual host's response (including resistance and immune status) play a crucial role in determining the progression of this condition [3, 4]. Periodontal diseases refer to infections linked to specific pathogenic bacteria that inhabit the subgingival region. Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans, at least two of these microorganisms, exhibit powerful virulence mechanisms and can infiltrate the gingiva. However, similar to many chronic infections, the development and course of periodontal infections are significantly influenced by local and systemic host conditions and risk factors. These factors significantly impact the host's resistance to periodontal organisms [5]. Systemic risk factors, as identified in recent large epidemiological studies, include diabetes mellitus and cigarette smoking. Additionally, individuals with acquired immunodeficiency syndrome (AIDS) are susceptible to periodontal disease, including severe and painful necrotizing forms. These systemic conditions significantly impact the development and progression of periodontal infections, emphasizing the importance of considering both local and systemic host factors in managing gum health. There is obvious link between psychoemotional stress and periodontal diseases [6, 7]. It is clear from evidence that stress reduces the flow of salivary secretions, which in turn can enhance dental plaque formation [8, 9].

Purpose of the article. This narrative review aims to summarize the scientific information on stress and depression concerning periodontitis, emphasizing the emerging role of neuroendocrine and neuroimmune mediators in the pathophysiology of inflammatory diseases.



Materials and methods

An analysis, comparison, and summarizing of information from modern scientific literature on the investigated problem was done. For the present study, an electronic search was done using MEDLINE (PubMed), Google Scholar and in open access journals which are published by Elsevier. For the search words and phrases such as: «stress», «endocrine system», «adrenal glands», «cortisol», «periodontal diseases» were used in various combinations. 202 articles were found, from which 29 were selected. The selected items include research and review articles. The search considered works published from 2010 until November 2023 by using the abovementioned key words as we want to include only up to date information. Only relevant literature in English from the electronic search was selected for the present review. The inclusion criteria are as follows: (i) full text journal articles written in English; (ii) books and book chapters written in English; (iii) scientific works published in 2010 and later (only for the chapter presentation of the main material of the study, because there we review these relevant papers). The exclusion criteria are as follows: (i) case reports (clinical trials); (ii) conference papers; (iii) materials published earlier than 2009; (iv) randomized controlled studies; (v) editorials.

(1) The search was carried out in MEDLINE (PubMed), using the keywords: «stress», «endocrine system», «adrenal glands», «cortisol», «periodontal disease» in various combinations. In total, 202 records were found.

(2) Co-authors analyzed 202 records for compliance with the inclusion and exclusion criteria. Scientific papers were distributed equally between authors for screening.

(3) All selected records were distributed among all authors for reading of the full text articles and preparation of the manuscript. The procedure is shown in Figure 1 in the PRISMA flowchart.



Fig. 1. PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) flow diagram of inclusion/exclusion criteria.

Presentation of the main material of the study

Stress induces both behavioral and biological reactions that activate the hypothalamus-pituitary-adrenal axis, which leads to an increase in the level of cortisol and pro-inflammatory biomarkers, which can be involved in the development of various diseases, in particular, the organs of the oral cavity (Figure 2). [11]. Glucocorticosteroids, including cortisol, have the effect of suppressing immunity. This suppression impacts secretory IgA, IgG, and neutrophil functions, all of which play a role in protecting against infections caused by periodontal organisms [12]. Specifically, secretory IgA antibodies may offer protection by reducing the initial colonization of these pathogens.



Fig. 2. The way psychoemotional stress affects periodontal tissues. (The figure is created by authors in BioRender.com application)

Periodontal diseases nowadays have a steady tendency to increase. The etiological factor of their occurrence is both local reasons and the combined action of exogenous and endogenous factors based on changes in the body's reactivity. It is also known that in modern conditions, psychoemotional stress is a premorbid background for the development of somatic pathology [13]. In the case of a stress reaction, microcirculatory disturbances are observed; the content of glucocorticoids, which have a catabolic effect, increases, and lipid peroxidation increases, which leads, among other things, to damage of periodontal tissues and inhibition of their regenerative processes [14].

Researchers proved that people who are under psychological stress are more prone to the development of periodontal diseases. Such people have slowed down the healing of connective and bone tissue, the apical migration of the connective epithelium, and the formation of a periodontal pocket [15, 16].This is facilitated by changes in the body's protective forces, which acquire an immunosuppressive effect, increasing disease susceptibility. Cytokines and other humoral mediators of inflammation are potent activators of the central stress response [17]. Glucocorticoids released under their influence can regulate the recruitment of immune cells to inflamed tissues to help the body cope with psychological stress and depression [18].Cytokines or matrix metalloproteinases are involved in periodontal destruction from the point of view of the host's inflammatory and immune response. Among them, interleukin (IL-6) is a potent pro-inflammatory cytokine closely related to periodontal destruction. It is produced in the body after exposure to immunological and psychological influences and plays a vital role in neuroendocrine and psychophysiological responses to stress [19, 20]. Under stress, saliva secretion decreases, and dental plaque formation increases. Neurotransmitters and neuropeptides, neuroendocrine substances that modulate the immune response to bacteria, are released. During emotional stress, the pH of saliva and sIgA (salivary immunoglobulin A) secretion changes significantly, and an increase of interleukin (IL-1) levels and cortisol levels in the gingival fluid is noted [21, 22]. periodontal pharmacotherapy stress dentistry

The effect of chronic stress on the content of pro-inflammatory and antiinflammatory cytokines in periodontal tissues in chronic experimental periodontitis was studied [23,24].It was proved that the balance between pro-inflammatory and anti-inflammatory cytokines is disturbed in stressed rats. When chronic generalized periodontitis is experimentally reproduced, the cytokine profile does not recover within fourteen days after the end of modeling the pathological process. Chronic stress creates conditions for the progression of chronic periodontitis [25, 26].

Numerous experiments proved that developing endothelial and mitochondrial dysfunction in the gum tissue accompanies chronic psychoemotional stress. This dysfunction can serve as the basis for the occurrence of periodontal disease due to a violation of microcirculation. As a result, the trophic function in the tissue and energy metabolism may be affected [27, 28]. People with chronic psychoemotional stress have structural changes in bone tissue, which indicate the development of destructive processes with disruption of the intercellular signaling system. These changes may lead to signs of cell necrosis. Ultrastructural changes in gum tissue and bone tissue can be the basis for the development of periodontitis in chronic psychoemotional stress and lead to tooth loss [29, 30]. The results of scientific research showed that chronic stress causes a typical complex of stress reactions in experimental animals: pathological changes in internal organs such as hypertrophy of the adrenal glands and involution of the thymus [31]. The scientists also noted the signs of catarrhal gingivitis: they visually detected dental plaque, swelling, and hyperemia of the gums with a pronounced vascular pattern and bleeding on a slight provocation. An increase in the content of secondary lipid peroxidation products in periodontal tissues accompanies chronic immobilization stress [9, 32]. Several authors note similar biochemical changes in oral fluid, blood, and periodontal tissues during acute immobilization and emotional pain stress in humans and animals. Reactive oxygen species can trigger a whole cascade of free radical oxidation reactions, the products of which have a toxic effect on cells and can be one of the pathologic factors that destroy periodontal soft tissues [33, 34].In addition, connective tissue structures are much less protected by antioxidant enzymes. Along with increased peroxide processes in periodontal tissues, some authors observed destruction of cell membranes, inhibition of collagen synthesis, increased resorption of bone tissue, blood circulation disorders [35]. Scientists found a significant increase in total collagenolytic activity in the periodontal soft tissues of rats with long-term emotional and pain stress. Polymorphonuclear leukocytes, fibroblasts, and macrophages are believed to cause gingival collagenase activity [36]. Prolonged exposure to stress activates collagenolysis, which causes damage to periodontal collagen fibers. It is known that the stress syndrome is accompanied by the labialization of lysosomes and the release of proteolytic enzymes, which leads to the development of hyperenzymemia [37]. Simultaneously, the activation of collagenolysis in animals subjected to emotional and pain stress observed a significant increase in the resorption of the alveolar process.



Conclusions from this study and prospects for further exploration in this direction

In summary, chronic stress negatively impacts periodontal health, highlighting the importance of addressing stress as part of overall well-being. Stress, in an acute or chronic form, affects not only our mental health but, due to several pathophysiological mechanisms, causes the development of pathological processes in periodontal tissues. Stress management is crucial to prevent and control periodontitis. Therefore, the study of the impact of stress on the development and course of periodontal diseases and the further development of appropriate schemes of prevention and rational pharmacotherapy is a promising and urgent task of today's dentistry.

Acknowledgments. The work is a fragment of inter-department scientific research work «Development and implementation of differentiated approaches of diagnosis, treatment and prevention of periodontal and oral mucosa diseases» (state registration number 0123U100071).



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26. Zemouri, C., Jakubovics, N. S., Crielaard, W., Zaura, E., Dodds, M., Schelkle, B., & Loos, B. G. (2019). Resistance and resilience to experimental gingivitis: a systematic scoping review. BMC Oral Health, 19, 1-18. https://doi.org/10.1186/s12903-019-0889-z

27. Dursun, E., Akalin, F. A., Genc, T., Cinar, N., Erel, O., & Yildiz, B. O. (2016). Oxidative stress and periodontal disease in obesity. Medicine, 95(12), e3136. https://doi.org/ 10.1097/MD.0000000000003136

28. Martinez-Herrera, M., Abad-Jimenez, Z., Silvestre, F. J., Lopez-Domenech, S., Silvestre-Rangil, J., Marquez-Arrico, C. F., ... & Rocha, M. (2020). Effect of non-surgical periodontal treatment on oxidative stress markers in leukocytes and their interaction with the endothelium in obese subjects with periodontitis: a pilot study. Journal of clinical medicine, 9(7), 2117. https://doi.org/10.3390/jcm9072117

29. Pupin, T. I., Honta, Z. M., Shylivskyy, I. V., Nemesh, O. M., & Burda, K. B. (2022). The role of adaptive-stress response in the pathogenesis of periodontal diseases. Wiadomosci lekarskie, 75(4 pt 2), 1022-1025. https://doi.org/10.36740/WLek20220420119

30. Saulin, M., Bolevich, S., Savateva-Liubiova, T., Sivak, K., & Silina, E. (2019). Peculiarities of free-radical processes and neuropsychological status in patients with chronic generalized periodontitis and possibility of correcting their impairments with antioxidant therapy. Serbian Journal of Experimental and Clinical Research, 20(2), 55-64. https://doi.org/ 10.2478/SJECR-2019-0034

31. Ball, J., & Darby, I. (2022). Mental health and periodontal and peri-implant diseases. Periodontology 2000, 90(1), 106-124. https://doi.org/10.1111/prd.12452

32. Lopes Castro, M. M., Nascimento, P. C., Souza-Monteiro, D., Santos, S. M., Arouck, M. B.,

Garcia, V. B., ... & Lima, R. R. (2020). Blood oxidative stress modulates alveolar bone loss in chronically stressed rats. International journal of molecular sciences, 21(10), 3728. https://doi.org/10.3390/ijms21103728

33. Warren, K.R., Postolache, T.T., Groer, M.E., Pinjari, O., Kelly, D.L. and Reynolds, M.A. (2014), Role of chronic stress and depression in periodontal diseases. Periodontal 2000, 64: 127-138. https://doi.org/10.1in/prd.12036

34. Marchetti, E., Monaco, A., Procaccini, L., Mummolo, S., Gatto, R., Tete, S., ... & Marzo, G. (2012). Periodontal disease: the influence of metabolic syndrome. Nutrition & metabolism, 9(1), 1-13. https://doi.org/10.1186/1743-7075-9-88

35. Saluja, H. M., Sachdeva, S., & Mani, A. (2021). Role of reactive oxygen species and antioxidants in periodontal disease. Journal of Cellular Biotechnology, 7(2), 125-140. https://doi. org/10.3233/JCB-210044

36. Sczepanik, F. S. C., Grossi, M. L., Casati, M., Goldberg, M., Glogauer, M., Fine, N., & Tenenbaum, H. C. (2020). Periodontitis is an inflammatory disease of oxidative stress: We should treat it that way. Periodontology 2000, 84(1), 45-68. https://doi.org/10.1111/prd.12342

37. Demkovych, A. (2023). Endogenous intoxication in development of experimental periodontitis of bacterial-immune genesis. FoliaMedica, 65(1), 149-154. https://doi.org/10.3897/ folmed.65.e71970



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24. Newman, M. G., Takei, H., Klokkevold, P. R., & Carranza, F. A. (2018). Newman and Carranza's Clinical Periodontology E-Book: Newman and Carranza's Clinical Periodontology E-Book. Elsevier Health Sciences.

25. Goyal, S., Gupta, G., Thomas, B., Bhat, K. M., & Bhat, G. S. (2013). Stress and periodontal disease: The link and logic!!. Industrial psychiatry journal, 22(1), 4. doi: 10.4103/ 0972-6748.123585

26. Zemouri, C., Jakubovics, N. S., Crielaard, W., Zaura, E., Dodds, M., Schelkle, B., & Loos, B. G. (2019). Resistance and resilience to experimental gingivitis: a systematic scoping review. BMC Oral Health, 19, 1-18. https://doi.org/10.1186/s12903-019-0889-z

27. Dursun, E., Akalin, F. A., Genc, T., Cinar, N., Erel, O., & Yildiz, B. O. (2016). Oxidative stress and periodontal disease in obesity. Medicine, 95(12), e3136. DOI: 10.1097/ MD.0000000000003136

28. Martinez-Herrera, M., Abad-Jimenez, Z., Silvestre, F. J., Lopez-Domenech, S., Silvestre-Rangil, J., Marquez-Arrico, C. F., ... & Rocha, M. (2020). Effect of non-surgical periodontal treatment on oxidative stress markers in leukocytes and their interaction with the endothelium in obese subjects with periodontitis: a pilot study. Journal of clinical medicine, 9(7), 2117. https://doi.org/10.3390/jcm9072117

29. Pupin, T. I., Honta, Z. M., Shylivskyy, I. V., Nemesh, O. M., & Burda, K. B. (2022). The role of adaptive-stress response in the pathogenesis of periodontal diseases. Wiadomosci lekarskie, 75(4 pt 2), 1022-1025. DOI: 10.36740/WLek20220420119

30. Saulin, M., Bolevich, S., Savateva-Liubiova, T., Sivak, K., & Silina, E. (2019). Peculiarities of free-radical processes and neuropsychological status in patients with chronic generalized periodontitis and possibility of correcting their impairments with antioxidant therapy. Serbian Journal of Experimental and Clinical Research, 20(2), 55-64. DOI: 10.2478/SJECR-2019-0034 '

31. Ball, J., & Darby, I. (2022). Mental health and periodontal and peri-implant diseases. Periodontology 2000, 90(1), 106-124. DOI: 10.1111/prd.12452

32. Lopes Castro, M. M., Nascimento, P. C., Souza-Monteiro, D., Santos, S. M., Arouck,

M. B., Garcia, V. B., ... & Lima, R. R. (2020). Blood oxidative stress modulates alveolar bone loss in chronically stressed rats. International journal of molecular sciences, 21(10), 3728. doi:10.3390/ijms21103728 '

33. Warren, K.R., Postolache, T.T., Groer, M.E., Pinjari, O., Kelly, D.L. and Reynolds, M.A. (2014), Role of chronic stress and depression in periodontal diseases. Periodontol 2000, 64: 127-138. https://doi.org/10.1111/prd.12036

34. Marchetti, E., Monaco, A., Procaccini, L., Mummolo, S., Gatto, R., Tete, S., ... & Marzo, G. (2012). Periodontal disease: the influence of metabolic syndrome. Nutrition & metabolism, 9(1), 1-13. https://doi.org/10.1186/1743-7075-9-88

35. Saluja, H. M., Sachdeva, S., & Mani, A. (2021). Role of reactive oxygen species and antioxidants in periodontal disease. Journal of Cellular Biotechnology, 7(2), 125-140. DOI 10.3233/JCB-210044

36. Sczepanik, F. S. C., Grossi, M. L., Casati, M., Goldberg, M., Glogauer, M., Fine, N., & Tenenbaum, H. C. (2020). Periodontitis is an inflammatory disease of oxidative stress: We should treat it that way. Periodontology 2000, 84(1), 45-68. DOI: 10.1111/prd. 12342

37. Demkovych, A. (2023). Endogenous intoxication in development of experimental periodontitis ofbacterial-immune genesis. FoliaMedica, 65(1), 149-154. DOI: 10.3897/folmed.65.e71970

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