Cytokine profile of oral fluid in case of traumatic fractures of the lower jaw and the presence of third molars in patients` oral cavity

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Abstract

Objective. To analyze the level of cytokines in the oral fluid of patients with traumatic fractures of the mandible in the presence of third molars, to establish the influence of the latter on the oral cavity homeostasis, to determine the most informative indicators.

Materials and methods. 82 people aged 18–60 years took part in the study, they were divided into 3 groups. Group 1 contained 43 patients with mandibular fracture and having more than two third molars. Group 2 consisted of 18 patients with mandibular fracture, without third molars. Group 3 included 21 people without a fracture of the mandible, who had more than two-thirds of the molars. Group 4 (control) contained the data of somatically and dentally healthy individuals, borrowed from special literature. The levels of IL-1β, IL-6, IL-8, and TNF-a in OF were determined using standard enzyme immunoassay kits. The data were processed statistically.

Results. A comparison of the indicators of groups 1 and 3 revealed a significant increase in the level of IL-6 z = 4.15 (H = 20.43; p = 0.0001) and the level of IL-8 z = 3.08 (H = 12.29; p = 0.0064) in patients with a jaw fracture. A considerable increase in IL-8 levels was determined in the individuals from group 2 compared with group 3 – z = 2.74 (H = 12.29; p = 0.0064).

The comparison of groups 1 and 4 in terms of TNF-a showed a tendency to a significant difference of z = 1.60 (H = 4.65; p = 0.19), and the data of group 2 in comparison with group 4 were significantly higher than z = 1.97 (H = 4.65; p = 0.19). Comparing the results of groups 3 and 4 with each other we revealed a considerable difference of z = 1.75 (H = 4.65; p = 0.19).

Conclusion. The profile of cytokines level in the OF indicates that the presence of third molars in the oral cavity in mandibular fractures affects the homeostasis of the oral cavity negatively, which is the reason for expanding the indications for their removal in order to prevent infectious and inflammatory complications.

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Introduction

Constant scientific and technological progress leads to an increase in injuries, and consequently, the number of traumatic injuries to the bones of the facial skull, including the lower jaw, increases. Attention is paid to the development of treatment and medical rehabilitation methods for traumatic fractures of the jaws by maxillofacial and dental surgeons [1]. However, despite the constant improvement of known methods, the development and introduction of new methods aimed at increasing the efficiency of specialized medical care to the population of patients with these lesions, the incidence of complications remains high, ranging 10–41 % [2; 3]. This indicates that the existing approaches to the treatment of this pathology and medical prevention of its complications at the present stage are insufficiently effective and that there are unaccounted factors that can have a negative impact on the homeostasis of the oral cavity and maxillofacial region and the patient’s body as a whole.

Notably, considering the epidemiological situation worldwide, one of the priority scientific directions is the development of methods for noninvasive diagnosis, forecasting the development and course of diseases, including surgical pathology of the maxillofacial region and neck. Currently, a promising area of scientific research is diagnostics and prognosis using body fluids obtained noninvasively. From this position, more specialists pay attention to the oral fluid (OF). This choice is because of the fact that its informative value in both somatic and dental pathology has been proven, and its sampling does not require invasive manipulations and can be performed for the required number of times [4].

There is a significant number of publications in the specialized literature, including periodical press sources and electronic resources, regarding the level of cytokine content in the biological media of the human body in somatic diseases and in surgical pathology of the maxillofacial region and neck [5; 6]. Some of the studies contain information about the level of cytokines in traumatic fractures of the mandible [7].

Cytokines are biologically active substances that are products of a large number of cells of various tissues and organs, produced by them during the entire period of life in response to any external influence, including pathogenic effects. They affect the proliferation, differentiation, and functional activity of target cells. Several variants of their biological activity have been identified, depending on the participation in the process of various intracellular systems that transmit signals from receptors and contribute to this. The realization of such signal transduction is conditioned by the peculiarities of specific target cells [8].

First, cytokines implement a local-level immune response that develops as a typical inflammatory reaction with all the relevant signs (i.e., edema, hyperemia, pain, fever, and dysfunction). Inflammation develops in response to the penetration of an infectious agent into the tissues of the macroorganism by invasion (during injury, surgery, trauma, etc.) with the obligatory participation of pro-inflammatory cytokines, including interleukin (IL)-1, IL-6, tumor necrosis factor (TNF), and chemokines [9].

Second, IL-8 is a glycoprotein (chemokine). Its main function is to ensure migration of cells of various types (e.g., leukocytes, monocytes, eosinophils, lymphocytes, etc.) to the inflammatory zone. One of its main characteristics is its ability to influence the endothelium of blood vessels, contributing to the activation of neutrophil adhesion to the surface of the blood vessels. Additionally, IL-8 induces chemotaxis of granulocytes, monocytes, and lymphocytes in the infectious–inflammatory focus. It activates the action of neutrophils, namely, their degranulation. Moreover, this glycoprotein promotes more active production of pro-inflammatory cytokines by mononuclear cells [10].

TNF is a pro-inflammatory cytokine that is produced by macrophages and monocytes. It has various functions and influences lipid metabolism, insulin resistance and coagulation, as well as corresponds to endothelial functions [11]. TNF activates the production of interleukins (IL-1, IL-6, and IL-8) and interferon-gamma and activates leukocytes. It is one of the factors that resist effects of intracellular parasites and viruses. Excessive production and increased TNF levels can lead to hemodynamic disorders and cytotoxic effects on body cells, which occur in various pathological processes [12; 13].

There are the results of the study of OF indicators in patients with traumatic jaw fractures in periodicals and specialized literature [14], including data from the analysis of immunologic indicators, including the level of cytokine content [2].

However, analysis of data from the specialized literature did not reveal evidence based on the principles of evidence-based medicine and did not confirm the effect of third molars in patients with traumatic mandibular fractures on OF cytokine profile and on oral homeostasis.

The abovementioned arguments demonstrate the relevance of the presented study and indicate the need to perform a targeted study of the profile of OF cytokines in individuals with traumatic fractures of the mandible in the presence of third molars and determine the effect of the latter on the homeostasis of the oral cavity and body as a whole.

This study aimed to analyze the level of cytokines in the oral fluid of patients with traumatic fractures of the mandible in the presence of third molars, establish the influence of the latter on the homeostasis of the oral cavity, and determine the most informative indicators.

Materials and methods

The study was conducted in compliance with the basic principles of bioethics, after the official positive conclusion of the bioethics commission of the educational institution “Belarusian State Medical University.”

The study included 82 individuals aged 18–60 years. Of these, 57 (70 %) were men and 25 (30 %) were women. Each participant personally signed an informed consent to participate in this study.

The criteria for inclusion were age ≥18 years and absence of injuries and somatic pathology (except for traumatic fracture of the jaw, for which they are undergoing treatment). The exclusion criteria were age <18 years and >60 years, injuries (except for a traumatic fracture of the jaw, for which they are undergoing treatment), somatic diseases, allergic reactions, presence of infectious and inflammatory processes in the maxillofacial region, oral mucosa
diseases, presence of amalgam fillings in the oral cavity, dental implants, and dentures. Table 1 presents the distribution of the indicated participants of the study in the selected groups.

 

Table 1

Distribution of examined patients in the selected groups

Selected groups of patients

Characteristics of the selected groups of patients

Absolute number of patients
in the selected groups

Proportion of
patients in each group relative to the total number of examined
patients, %

Group 1

Patients with a fractured mandible and having more than two third molars in the oral cavity

43

52

Group 2

Patients with mandibular fracture who have no third molars in the oral cavity

18

22

Group 3

Patients without a fracture of the mandible and having more than two thirds of molars in the oral cavity

21

26

Group 4
(control)

Somatically and dentitically healthy individuals (data on the level of cytokines in oral fluid are borrowed from sources of special literature [15; 16])

–

–

 

Traumatic fracture of the mandible was diagnosed based on the clinical picture and confirmed by radiology [17].

The frequency of localization of the fracture line in individuals with traumatic injuries of the lower jaw (groups of patients 1 and 2) was distributed as follows: canine region, 17 (27.9 %); area of the jaw body, 23 (37.7 %); and area of the angle of the jaw, 21 (34.4 %).

The listed groups of patients were comparable in sex (cp2 = 209.48; р = 0.00), age (cp2 = 17.53; р = 0.001) and somatic and dental status. All the individuals involved in the study underwent clinical and laboratory examination [18]. Table 2 provides a complete list of the research methods used in the study.

 

Table 2

The research methods used in the work and their characteristics

Research methods used
 in the work

Characteristics of the research methods used

Clinical research methods

Collection of complaints, history of life, history of disease, and external examination

Traditional data collection algorithms

Examination of the oral cavity

Determination of caries index, fillings, extracted teeth (CPI), calculation of caries intensity level (CIL); determination of hygienic index O-HIS; and complex periodontal index (CPI) by P.A. Leus (1988)

Laboratory research methods

Determination
of IL-1b, IL-6, IL-8, and TNF-a levels in the oral fluid

Oral fluid for the analysis of cytokine levels was collected from the participants in the period from 8.00 to 11.00 (to exclude the effect on the result of circadian biological rhythms of participants), on an empty stomach, in sterile test tubes, no earlier than 30 minutes after brushing the teeth. Samples were labeled and stored in a biological freezer at -70°C until processing.
After thawing, samples were separated into supernatant and sediment
fractions by centrifugation. The supernatant fraction was examined.
Cytokine levels in the oral fluid were determined using standard enzyme immunoassay kits according to the recommendations of the literature [18]; the result was expressed in pg/ml

Statistical research methods

The obtained data were processed statistically using the Statistica 10.0 application software package

Considering that there was a different distribution of the trait from the normal one, nonparametric statistical processing was used. Hence, the
median (Me), lower (LQ), and upper (UQ) quartiles were calculated.
The significance of the indicators of the compared groups of patients was determined by the Kruskal – Wallis criterion (H). Analysis of qualitative data was performed according to the Pearson criterion c2. The result was considered significant at p < 0.05

 

Results and discussion

The examined patients had a high CIL. The hygienic index of O-HIS was 2.4 ± 0.2, which indicated an unsatisfactory result. The CPI data were 3.4 ± 0.1 and indicated an average severity of periodontal lesion. The dental examination data were consistent with those in the studies by Zoirov et al. and Ushnitsky et al. [19; 20] and indicated that the groups compared in the study had no significant differences in sex, age, and somatic and dental status and therefore were comparable.

The level of IL-1b in group 1 OF was 14.15 (9.85–23.30) pg/ml.

The IL-6 index was 16.95 (7.05–85.00) pg/ml. The level of IL-8 in the studied biological medium was 1705.0 (690.0–1965.0) pg/ml. The TNF-a index of oral fluid was 7.5 (5.8–9.2) pg/ml.

Furthermore, the levels of cytokines in the natural biological environment of the oral cavity of group 2 were as follows: IL-1b, 12.10 (9.30–17.60) pg/ml; IL-6, 9.70 (5.60–250.00) pg/ml; IL-8, 1930.0 (1440.0–1960.0) pg/ml; and TNF-a, 8,7 (7.5–9.8) pg/ml.

The indices of the studied OF cytokines in group 3 were as follows: IL-1b, 19.00 (10.25–30.90) pg/ml; IL-6, 5.30 (4.40–7.10) pg/ml; IL-8, 341.0 (150.0–1450.0) pg/ml; and TNF-a, 8.1 (6.4–10.4) pg/ml.

Moreover, the results of the level of OF cytokines of group 4 (control) were the following: IL-1b, 0.00 (0.00–1.30) pg/ml; IL-6, 0.00 (0.00–0.70) pg/ml; IL-8, 386.2 (287.8–538.9) pg/ml; and TNF-a, 0.0 (0.0–0.0) pg/ml [15; 16]. A comparative assessment of the results of the level of OF cytokines in groups 1 and 2 did not reveal significant differences. When comparing the indices of groups 1 and 3 according to the criterion for multiple Kruskal – Wallis comparisons, significant increases were found in the level of IL-6 (z = 4.15 [H = 20.43; p = 0.0001]) and IL-8 (z = 3.08 [H = 12.29; p = 0.0064]) in participants with fractures of the mandible (Figs. 1 and 2).

 

Fig. 1. Box graph of comparative comparison of the level of IL-6 content in the studied biological fluid of the examined patients

 

Fig. 2. Box graph of comparative comparison of the level of IL-8 content in the studied biological fluid of the examined patients

 

The study found an increase in the IL-8 index of group 2 when compared with the data of group 3 according to the Kruskal – Wallis criterion (z = 2.74 [H = 12.29; p = 0.0064]). According to Prokhodnaya and Gaivoronskaya, increased IL-6 and IL-8 levels in the oral fluid can contribute to the development and activation of inflammatory and destructive processes [21], including osteomyelitis. Additionally, experts revealed that an increase in IL-8 level in OF indicates the activation of local immunity in the area of a bone wound and prevalence of an infectious and inflammatory process [2; 15]. A comparative assessment of the results of groups 1 and 4 regarding TNF-a content in OF based on the Kruskal – Wallis criterion revealed a significant difference (z = 1.60 [H = 4.65; p = 0.19]), and a comparison of the data from groups 2 and 4 showed a significantly higher result in patients with traumatic fracture of the mandible according to the specified criterion (z = 1.97 [H = 4.65; p = 0.19]). When comparing the results of groups 3 and 4 according to the Kruskal – Wallis criterion, a significant difference was noted (z = 1.75 [H = 4.65; p = 0.19]).
A comparative assessment of the TNF-a level in the oral fluid of the examined groups is presented in Fig. 3.

 

Fig. 3. Box graph of the comparative comparison of the TNF-a content in the studied biological fluid of the examined patients

 

Moreover, in examining the specialized literature on the issue under discussion, several studies demonstrated that an increase in TNF-a level in the body fluids of a patient with a traumatic bone fracture may indicate the development of inflammatory and destructive complications [22; 23].

The results provide reason to consider the immunological parameters of IL-6, IL-8, and TNF-a as additional diagnostic and prognostic tests for fractures of the mandible. Moreover, the results of the level of IL-8 and TNF-a reflect the effect on the homeostasis of the oral cavity of the presence of third molars in the latter, including in fractures of the mandible.

Conclusions

An increase in IL-8 and TNF-a levels in the oral fluid indicates that the presence of third molars in the oral cavity in patients with fractures of the mandible negatively affects the homeostasis of the oral cavity, which is the basis for expanding the indications for their removal in group 1 patients during primary surgical wound treatment to prevent infectious–inflammatory complications, as well as in individuals who experience traumatic activities that could potentially belong to group 3.
Considering the fact that an increase in the level of cytokines in the oral fluid in persons with traumatic jaw fractures can be regarded as a marker of the development of inflammatory and destructive complications, in patients in this category, even in the absence of third molars in the oral cavity (group 2), it is crucial to resolve the need for and scope of correction of therapeutic measures (secondary surgical treatment and/or modification of the means and regimen of antibacterial therapy).

×

About the authors

I. O. Pohodenko-Chudakova

Belarusian State Medical University

Author for correspondence.
Email: ip-c@yandex.ru
ORCID iD: 0000-0002-0353-0125

DSc (Medicine), Professor, Head of the Department of Dental Surgery

Belarus, Minsk

Ali Thergam Abdulameer Ali

Belarusian State Medical University

Email: ip-c@yandex.ru
ORCID iD: 0000-0003-4142-5817

Postgraduate Student of the Department of Dental Surgery

Belarus, Minsk

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2. Fig. 1. Box graph of comparative comparison of the level of IL-6 content in the studied biological fluid of the examined patients

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3. Fig. 2. Box graph of comparative comparison of the level of IL-8 content in the studied biological fluid of the examined patients

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4. Fig. 3. Box graph of the comparative comparison of the TNF- content in the studied biological fluid of the examined patients

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