Registration of thermal images of dead teeth to identify odontogenic infection foci

Abstract

Infrared thermal imaging (IRT) remotely and contactless maps the temperature on the examined surface, recording the distribution of infrared radiation emitted by each body whose temperature is higher than absolute zero. The aim of the study was to evaluate the usefulness of thermography in the assessment of asymptomatic infection foci in patients with high systemic infection. The 150 cases diagnosed based on roentgenograms, divided into 6 groups of diagnosed odontogenic lesions, along with a control group. Thermal imaging was performed with a FLIR Systems T1020 thermal camera. Thermal image analysis was performed using ThermaCAM Researcher Pro 2.10, MS Office Excel 2022 and Statistica 10. The periapical areas of selected dead teeth were selected as areas of interest. The Mann Whitney’s U test showed statistically significant (p < 0.001) differences in average temperature between each patient’s and healthy group. Depper’s analysis showed statistical significance also between the ZM and BZ groups (p = 0.004). Moreover, obtained results may also suggest that thermal imaging can be useful in identify odontogenic infection foci. The thermal asymmetry of periapical tissues of teeth differentiates dead from living teeth, as well as individual pathologies related to the process of gangrenous pulp decay. Thermographic mapping is a promising diagnostic technique that can detect asymptomatic inflammations that carry the risk of infection of the entire body.

Introduction

Infrared thermal imaging (IRT) is gaining increasing use as a non-ionizing diagnostic tool in medicine. It maps the temperature on the tested surface remotely and without contact, recording the distribution of infrared radiation emitted by each body whose temperature is higher than absolute zero^1–4. Mapping a selected area of interest is a key element in the thermographic analysis process because it allows you to focus on a specific area that is important for diagnosis or monitoring. Thermographic mapping of the periapical area of teeth is a promising diagnostic technique that can detect asymptomatic inflammations that carry the risk of infection of the entire body^5–9.

Odontogenic infections can affect a person’s overall health. Spreading through continuity, they cause the invasion of adjacent anatomical spaces. The shedding of microorganisms into the blood from a primary, asymptomatic focus in the oral cavity may cause systemic infections and inflammatory changes in organs distant from the oral cavity^10–19 Therefore, a quick, non-invasive and effective diagnostic method for silent lesions is being sought as an alternative or complement to X-ray diagnostics.

The aim of the study is to assess the usefulness of thermography for the diagnosis of asymptomatic infection foci in patients at high risk of systemic infection. The work is a continuation of research after developing an original method of intraoral measurements.

Material and method of clinical examination

This study was conducted at the Department of Craniofacial Surgery, Silesian Medical University, from September to December 2021 and again from September to December 2023. Ethical approval for the study was obtained from the Ethical Committee of the Silesian Medical University (approval number PCN/CBN/0052/KB1/67/I/22).

For the research, patients were included who were diagnosed with dental pathology based on clinical and radiographic examination. A key element was to compare the own introduced early and non-invasive diagnostic procedure using thermal imaging with physical assessment and analysis of each patient’s medical records, including laboratory and X-ray examination.

The procedure relies on preliminary colling of the gums due to keep mouth open for 30 s before thermal imaging what was introduced in paper⁸. Such situation leads to cool the teeth vicinity what enhances skin temperature between symmetrical teeth and make possible to find and differentiate the asymptomatic odontogenic tissue pathologies.

Patients with asymptomatic odontogenic tissue pathologies identified on clinical or radiographic examination, with the presence of a healthy tooth on the opposite side, were eligible for the study. The study included adult patients of both sexes with associated medical conditions. Among the general burdens, the most common diseases were hypertension, diabetes, chronic kidney disease, infective endocarditis, atrial fibrillation, heart valve defects, leukemia, thrombocytopenia, lymphoma, multiple myeloma, Hashimoto’s disease, optic neuritis, vitritis, osteoporosis. A total of 150 cases were exanimated in the study. In the clinical examination, asymptomatic pathologies diagnosed based on a plain roentgenogram were divided into 6 groups:

1. Dead teeth properly treated with root canal without periapical changes endo BZ—69

2. Dead teeth, properly treated with root canal, with periapical changes endo ZZ—23

3. Dead teeth after root canal treatment with incomplete endo roots NP—9

4. Foreign bodies in the alveolar recess of the body FB—9

5. Teeth or roots with pulp in a state of gangrenous pulp decay ZM—5

6. Healthy volunteers C—35

All allergies, medications used, and consumption of caffeine, alcohol and other substances were identified. Temperature, blood pressure and heart rate were measured, and height and weight were measured.

The focus was on a detailed assessment of periodontal tissues, performing a basic periodontal examination using a probe; a probing diagram at six points around the tooth throughout the dentition. Pointing out areas with bleeding, furcations and tooth mobility. The oral mucosa was examined. All clinically suspicious teeth were subjected to diagnostic tests.

Radiological examinations included both panoramic and intraoral radiographs. If necessary, the patient was referred for additional sinus X-rays or cone beam computed tomography (CBCT).

Thermographic investigation

The thermal imaging was performed with a FLIR Systems T1020 thermal camera. The temperature of the room in which the measurements were taken was a stable 23 ± 1 [°C] and the humidity was 50%. The emissivity of the skin was set to 0.98²⁰. The thermal imaging camera was positioned perpendicular to the imaging surface and the distance from the patient was 0.4 ± 0.05 m in accordance with the standards for thermal imaging diagnostics in medicine.

Prior to the study, each patient was acclimatized to the room temperature for about 20 min with the aim²⁰. During this time physical activity should have been reduced to a minimum. A few hours before the measurements were taken, volunteers were advised not to consume warm drinks or meals. Patients were in a sitting position, then their head was immobilized with the mouth open and lips open (Fig. 1). Before immobilization, the patient was asked to rinse his mouth with water at room temperature for 1 min. Measurements taken include the anterior teeth of the maxilla or mandible. The thermal images include the ‘diseased’ teeth and their monotone teeth on the opposite side, which were used for comparison. Due to the difficult imaging conditions, the molar teeth were excluded from the study.

Fig. 1.

The scheme of thermal imaging showing angels and planes followed by investigators.

Statistical analysis

Thermal images analysis was performed using ThermaCAM Researcher Pro 2.10 software, where areas of interest (ROI, or Region of Interest) were selected. These areas included the periapical zone of the selected teeth and their counterparts on the opposite side. The average temperature was read from the lesion areas, which was always calculated as the average of all pixels in the selected area.

The results obtained were then collected, and statistical analyses were performed using the STATISTICA 10 program. For each analysis, the Shapiro–Wilk test was performed to check the type of distribution of measurable features. We checked whether the distribution of the variables was normal and if the variances were homogeneous, what has been done by using the Levene’s test. Based on those positive results, it was decided that parametric tests should be performed.

When the essential assumptions for the parametric tests were not met, nonparametric tests were used including the Mann–Whitney test for two comparing groups and for analysis of more than two groups – ANOVA Kruskal Wallis test and consequently post hoc tests. Data are expressed as the mean and median values ± standard deviation (SD) and standard error (SE). The level of significance was p < 0.05. The results are presented in box graphs. The mean temperature values from the periapical areas of the suspect and control teeth were compared. In addition, the differences between the mean temperature values between the ‘suspect’ and control teeth were calculated for the patient group and the control group.

Results

The thermal images of the representative patient’s periapical area of teeth obtained from all studied groups are presented in Figs. 2, 3, 4, 5, 6, respectively. Collected thermal images present two sides of the jawbones for every patient and the dental intrathecal probe at the periapical area for symmetrical teeth from which one is suspicious of odontogenic infection foci.

Fig. 2.

The representative patient’s thermal image from the dead teeth properly treated with root canal without periapical changes endo group named BZ.

Fig. 3.

The representative patient’s thermal image from the dead teeth properly treated with root canal with periapical changes endo group named ZZ.

Fig. 4.

The representative patient’s thermal image from the dead teeth after root canal treatment with incomplete endo roots group named NP.

Fig. 5.

The representative patient’s thermal image from the foreign bodies in the alveolar recess of the body group named FB.

Fig. 6.

The representative patient’s thermal image from the teeth or roots with pulp in a state of gangrenous pulp decay group named ZM.

The main goal of the study is to assess the usefulness of thermography for the diagnosis of asymptomatic infection foci in patients at high risk of systemic infection. That is why the average temperature differences between symmetrical teeth root vicinity has been taken into consideration as a primary sign of the health problem.

It is important to point attention to every pair of the thermal imaging and realize that there is temperature asymmetry between pointed by dental intrathecal probe of periapical area of teeth. Moreover, thermal asymmetry obtained for the studied groups of patients seem to differ.

It is known that the thermal asymmetry in human body has been found as a diagnostic sign of different illnesses and not only in the stomatology^5,8,9,21,22.

For better insight into the problem and for take into consideration not only the qualitative but lso quantitative parameters the statistical analysis has been performed.

As a first step the average temperature differences between symmetrical teeth root vicinity for all studied groups of patients and the of the control one has been checked and the results are presented in Fig. 7.

Fig. 7.

The average temperature differences between symmetrical teeth root vicinity obtained for all studied groups of patients and the of the control one.

Mann Whitney’s U test showed the statistically significant (p < 0.001) differences for the average temperature between every control group and healthy. Depper analysis showed the statistically significance also between groups ZM and BZ (p = 0.004) what is presented in Fig. 8.

Fig. 8.

Median of the temperature difference obtained for groups ZM and BZ.

The median temperature difference obtained for ZM is nearly 2.5 times higher than obtained for BZ. So, there is statistical difference of thermal asymmetry observed between not only all patients’ groups and healthy (what is clearly seen in Fig. 7) but undoubtedly between teeth or roots with pulp in a state of gangrenous pulp decay and dead teeth properly treated with root canal without periapical changes endo groups.

Moreover, the differences tendency can be seen for pairs of BZ and ZZ, ZZ and ZM as well as FB and ZM, however the p value did not meet the statistically significance and the obtained values for mentioned groups were 0.052, 0.056 and 0.06, respectively. Such results may show useful of thermal diagnostic in distinction between different illnesses when the study groups for these lesions will be much bigger.

Taking into consideration quite big standard deviations in obtained temperature results the median comparison seems to be good illustration for thermal characterization of all studied groups of patients what is presented in Fig. 9.

Fig. 9.

Median of the temperature difference obtained for all studied groups and the healthy one.

The median of the temperature difference obtained for all studied groups and the healthy give not only confirmation of obtained statistically significance differences between healthy and all patients, between Dead teeth properly treated with root canal without periapical changes endo and teeth or roots with pulp in a state of gangrenous pulp decay groups but also may bring some important tendencies observed for other illnesses temperature characteristic. It can be clearly seen that the median of temperature difference obtained for group of dead teeth properly treated with root canal with periapical changes endo as well as foreign bodies in the alveolar recess of the body group in comparison to dead teeth, properly treated with root canal with periapical changes endo is two times higher. Moreover, this parameter calculated for group of teeth or roots with pulp in a state of gangrenous pulp decay is even 2.5 times higher than dead teeth properly treated with root canal without periapical changes endo group and group with foreign bodies in the alveolar recess of the body. Such results may suggest that increase the numbers of the patient’s groups may bring statistically significance temperature parameters differences especially that the p values obtained for the studied cases are very close to the 0.05 what was mentioned above.

Discussion

The focal infection theory (FIT) posits that bacteria and/or bacterial toxins, and metabolic byproducts can enter the systemic circulation from clinically asymptomatic lesions containing pathogenic bacteria and travel to distant parts, initiating chronic metastatic disease in these organs^10–13.

The relationship between oral health and systemic health appears to be more complex than the classical theory of focal infection suggests. Microorganisms in the oral cavity form a complex ecosystem, having the ability to form biofilms in which they interact with each other and react with the host’s immune system. Bacteria that cause odontogenic infections are part of the oral microbiome and settle in the dental plaque on the tooth surface and do not cause disease. When the balance between the host and the microorganisms is disturbed, they behave like pathogens causing infection, contributing to the development of caries, gingivitis and periodontitis^14–16.

In recent years, extensive research in the field of periodontology has clarified these relationships and introduced the term “periodontal medicine” to describe the role that periodontitis plays in exacerbating or initiating systemic diseases¹⁰.

Correlations have been observed between periodontitis, which affects the level of mediators of the inflammatory cascade, contributing to the destabilization of atherosclerotic plaque and carrying the risk of cardiovascular complications. There is evidence to suggest that periodontitis may be associated with osteoporosis, diabetes, atherosclerosis, rheumatoid arthritis, pregnancy-related complications, lung disease, pancreatic cancer, chronic kidney disease, obesity and Alzheimer’s disease, and metabolic diseases^10–28.

The source of infection should also be found in dead teeth with gangrenous pulp, remaining roots, cysts, granulomas, and partially impacted teeth. Most systemic diseases are undoubtedly multifactorial in nature, however, endodontic infections: teeth treated with root canals with good therapeutic effects and those complicated with periapical granulomas may be the initiating factor^{10–13,23,24}. The endodontic community has steadfastly rejected an infected root canal as a cause of long-term non-infectious disease. There is undeniable evidence that treated periapical infections can cause long-term disease by releasing bacteria and bacterial products into the circulation¹⁰.

Peciuliene’s research has shown that inflammation of periapical tissues occurs in 43.1% of teeth with a filled root canal, and only 28.6% of teeth meet the criteria for acceptable root canal filling. The results of this study indicate that inadequate canal fillings were more often associated with an increased incidence of periapical inflammation²⁷. Recent reports indicate that the bidirectional relationship between the development of periapical inflammation and some common diseases, such as cardiovascular lesions and diabetes, is already well documented. Periapical inflammation is a local inflammatory event that occurs in response to endodontic infection. This stimulates the production of pro-inflammatory mediators that penetrate blood vessels and attract defense cells to the site of injury. In this way, the spread of these inflammatory modulators can trigger an immune response and impact the patient’s overall condition. Conversely, systemic diseases may also modulate the inflammatory response to the local lesion, increasing periapical tissue destruction. Certain systemic conditions may predispose to more intense inflammation, which results in increased bone loss and delayed healing in the case of periapical inflammation²⁷.

The most common cause of pulp and periapical tissue pathology is caries. As the carious lesion progresses, the pulp undergoes histological and morphological changes, causing an inflammatory reaction. If the pulp is treated properly, it returns to a healthy state. Acute pulpitis is symptomatic and chronic pulpitis is asymptomatic. These two pulp diseases require endodontic treatment, which, if not performed, may result in the extension of the lesion beyond the tooth apex, lead to disease of the periapical tissues and cause distant diseases by releasing bacteria and bacterial products into the circulation^6,27,29.

Accurate diagnosis of inflammation requires clinical and radiological tests, such as periapical or panoramic radiographs, cone beam computed tomography (CBCT), and even histological examination, if necessary. Symptomatic odontogenic infections are almost always diagnosed based on the history of the disease along with clinical and radiographic examination. Pain with or without swelling is usually the first signal of a developing infection²⁸.

Asymptomatic outbreaks pose a significant problem, especially in patients at high risk of odontogenic infections, i.e. patients with systemic diseases. Suspecting that dental pathologies classified based on radiological examination are characterized by variable metabolism and blood supply. They can produce a thermal response of the affected tissues and also show thermal asymmetry between symmetrical examination areas, i.e. a dead tooth and an identical healthy tooth on the opposite side. We have implemented thermal imaging diagnostics.

Infrared cameras could measure infrared radiation, which results in the generation of thermal images in which each pixel corresponds to a different temperature value. Mapping a selected area of ​​interest can be used to obtain physiological information about the area in question.

In the literature, there are attempts to identify odontogenic pathologies using thermography, assessing the vitality of the pulp in front teeth, differentiating dead teeth from healthy ones⁶ and differentiating chronic from acute inflammations⁵. We also see the initial development of intraoral examination protocols²⁹. The authors agree that infrared thermography is a promising alternative diagnostic technique when tests using ionizing radiation are inadvisable^5,8,29. The lack of standardization and unification of thermal imaging diagnostics prompted us to develop our own method⁸. Even though the current level of knowledge directs diagnostics towards the assessment of mediators of inflammation of molecular pathways³⁰. Thermal imaging is gaining popularity thanks to its non-invasiveness, speed and precision of research at low costs.

The scope of our research also included the alveolar recess of the maxillary sinus, where we detected asymptomatic foreign bodies resulting from endodontic treatment of teeth in this area. The obtained results showed a significant difference between the mean temperature difference of the sinus with the foreign body and the opposite sinus. After removing the foreign body from the sinus lumen, the temperature showed a dynamic decrease over time. The results of our study were published in a previous report³¹, and the problem of various foreign bodies in the lumen of the maxillary sinus is an observed iatrogenic pathology³².

Bearing in mind that thermal asymmetry in the human body is considered a diagnostic symptom of various diseases, average temperature differences were assessed between the symmetrical areas around the roots of dead and symmetrical healthy teeth. The observed significant differences in these areas prompted the authors to conduct further research, namely, to assess in which pathologies the average temperature difference is the largest. The research clearly showed that there are the greatest differences between teeth or roots with pulp in a state of gangrenous decay and dead teeth properly treated with root canal treatment without periapical changes. Going further, this parameter was assessed between individual dental pathologies, concluding that for the group of teeth or roots with pulp in a state of gangrenous decay, it is up to 2.5 times higher compared to dead teeth properly treated with root canal treatment without periapical changes and the group with foreign bodies in the alveolar recess of the maxilla. This fact proves that teeth with dead pulp carry a greater risk of infection than teeth properly treated with root canal treatment, without or with periapical lesions or foreign bodies in the alveolar recess of the maxillary sinus. The presented research provides valuable information about physiological processes occurring asymptomatically in tissues. They may initiate or maintain inflammation, leading to focal infection. Based on our own research and published and analyzed scientific reports, it can be concluded that infrared thermography is an auxiliary tool in dental diagnostics and useful in monitoring and examining therapeutic effects. Such results may also suggest that thermal imaging can be useful in identify odontogenic infection foci. The study did not include thermal assessment of periodontal tissues. However, we are deeply convinced that bacterial infection in the gingiva and periodontium causing increased blood flow leads to an increase in temperature and thus produces a thermal image. This topic requires research, standardization of techniques and interpretation of results.

Moreover, authors realize that the sample size should be calculated considering the maximal error, fraction size as well as population. Authors also have knowledge that polish population is about 38 million of people and each year about 30 million of stomatology interventions are being done. Moreover about 50% from these 30 million procedures have been performed for patients with pain which might be correlated with earlier odontogenic infection foci. Such logics may lead to about 15 million of ill patients. It is obvious that it is very big population and probably it is much lower. One way or another taking account presented reasoning the required sample size should be as 384 cases. However, our research is still ongoing, and we plan to increase the number of patients in the future, but due to the pandemic period, it was very difficult so decided to finish the first study with 150 qualified patients tested during the same year period in two years described in the materials and methods.

IRT is an alternative or complementary examination in cases where X-ray diagnostics is not indicated or impossible due to the general health condition of the patient. Patients with severe odontogenic sepsis who are patients of intensive care units, oncology wards or pregnant women can safely be prescribed a non-invasive thermographic examination of the oral cavity, using a thermal imaging camera, which will be equipped with a dentist consulting patients with systemic burdens.

Conclusion

Thermal imaging enables the measurement of thermal changes in areas of interest, providing information about ongoing physiological processes.

Thermal asymmetry of the periapical tissues of teeth differentiates dead teeth from living ones, as well as individual pathologies related to the process of gangrenous decay of the pulp.

Infrared thermography is an auxiliary tool in the assessment of odontogenic infection foci, as evidenced by our own research and numerous scientific reports.

Author contributions

Measurement, D.W.-K. and I.N.; writing—original draft preparation, D.W.-K. and A.M.; writing—review and editing, D.W.-K. and A.CH.; conclusions, D.W.-K. and A.CH.; discussion review, D.W.-K. and A.CH.; project administration, I.N.; data curation, A.M., software, A.CH.; formal analysis, A.M.; supervision, A.S., D.W.-K. and I.N. All authors reviewed the manuscript.  Informed consent was obtained from all subjects involved in the study.

Data availability

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

Competing interests

The authors declare no competing interests.

Ethics approval and consent to participate

The study was conducted in accordance with the Declaration of Helsinki and was approved by the Ethics Committee of the Medical University of SilesiaNo. PCN/CBN/0052/KB1/67/I/22.