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Published online 2010 May 7. doi: 10.3390/s100504700
PMID: 22399901
This article has been cited by other articles in PMC.
Abstract
Medical infrared thermography (MIT) is used for analyzing physiological functions related to skin temperature. Technological advances have made MIT a reliable medical measurement tool. This paper provides an overview of MIT’s technical requirements and usefulness in sports medicine, with a special focus on overuse and traumatic knee injuries. Case studies are used to illustrate the clinical applicability and limitations of MIT. It is concluded that MIT is a non-invasive, non-radiating, low cost detection tool which should be applied for pre-scanning athletes in sports medicine.
Keywords: thermal imaging, injury management, knee, infrared sensor technology
1. Introduction
Medical infrared thermography (MIT) provides a non-invasive and non-radiating analysis tool for analyzing physiological functions related to the control of skin-temperature. This rapidly developing technology is used to detect and locate thermal abnormalities characterized by an increase or decrease found at the skin surface. The technique involves the detection of infrared radiation that can be directly correlated with the temperature distribution of a defined body region [1].
An injury is often related with variations in blood flow and these in turn can affect the skin temperature. Inflammation leads to hyperthermia, whereas degeneration, reduced muscular activity and poor perfusion may cause a hypothermic pattern []. There are several applications of MIT in the field of human medicine, such as neurological disorders [3], open- heart surgery [4], vascular diseases [], reflex sympathetic dystrophy syndrome [], urology problems [] and mass fever screening []. Much research has been focused on the successful evaluation of breast cancer []. According to Ng [10] breast thermography has achieved an average sensitivity and specificity of 90%. He reported that an abnormal breast thermogram is a significant biological marker for breast cancer. One possible explanation is that increased blood flow due to the vascular proliferation that results from angiogenesis is associated with tumors []. Reduced skin temperature has also been implicated in musculoskeletal disorder (MSD). In fact, a cold skin pattern around ankle sprains indicates a poor prognosis and a long recovery time [12].
Infrared sensor technology also contributes to the field of injury management in athletic animals [–]. Anatomical and physiological similarities between animals and humans may imply that modern infrared sensor technology can provide significant information for the functional management of injuries in human athletes. However, there is scant scientific evidence of its successful application in the field of human sports medicine.
High performance training pushes the locomotor system to the edge of its anatomical and physiological limits. The knee is a weak link and is the most frequently affected joint in sports. Knee injuries are common in skiing and sports that involve jumping and abrupt direction changes []. Current trends indicate that in Austria, one of the top ski countries, the number of participants in competitive alpine skiing is greatly increasing, triggering a proliferation of knee injuries [18]. The incidence of long-term effects, such as osteoarthritis, are alarming.
These injuries usually involve a long, costly rehabilitation period and are often career-ending for athletes. The need for further research in the field of injury prevention and management is crucial to counteract severe skiing injuries.
2. International Status of Medical Infrared Imaging
MIT has been recognized by the American Medical Association council as a feasible diagnostic tool since 1987 and was recently acknowledged by the American Academy of Medical Infrared Imaging. Various groups and associations promote the proper application of thermal imaging in the practice of sports medicine. These groups include the European Association of Thermology, the United Kingdom Thermography Association, and the Northern Norwegian Centre for Medical Thermography, the American Academy of Thermology and the German Society of Thermography and Regulation Medicine (DGTR) as one of the oldest medical thermography society. The overall aim of these groups is to further improve reliable standardized methods and to develop appropriate protocols for clinical application.
The usefulness of MIT in sports medicine has been noted often []. However, some doubts about the technology highlight the necessity of doing further research. The major argument is whether MIT can accurately determine thermal variations to enable sufficient quantitative analyses []. Proponents of MIT state that “state-of-the-art” computerized systems using complex statistical data analysis ensure high quality results [] and that thermal sensitivity has increased, creating a new dimension that should be exploited and applied [22].
The absence of a standardized reference images is also a problem [23]. A research group from the University of Glamorgan is currently conducting research to determine “normal” thermograms by creating an “Infrared Atlas of Normal Human Skin Temperature Distribution”. Well-designed research studies can address these issues and help to resolve them.
3. Principles and Technique of Infrared Thermography
3.1. Electromagnetic Spectrum
There are several medical imaging modalities within the electromagnetic spectrum, which is defined as the range of electromagnetic radiation frequencies. Depending on their physical principles, these various techniques mainly provide anatomical information.
MIT is essentially a digital two-dimensional imaging technique that provides data about the physiology of tissues [24]. Unlike most diagnostic modalities, MIT is non-invasive. The question is whether physiological images can change prior to anatomic disruption. Specific software makes it possible to incorporate anatomical and physiological information by image fusion, which helps to localize the affected area and extent of the injury.
All images are obtained through the energy from the human tissue, leading to a classification based on the energy applied to the body. The energy content of the emission is related to the wavelength of the radiation.
Regarding the spectral region, human skin is a black body radiator with an emissivity factor of 0.98 [] and is therefore a perfect emitter of infrared radiation at room temperature. Planck’s law describes the characteristics of infrared radiation emitted by an object in terms of spectral radiant emittance [26].
Formula 1. Planck’s radiation law.
- H (Planck’s constant) = 6.6256 × 10−34 Js
- K (Boltzmann’s constant) = 1.38054 × 10−23 WsK−1
- C (velocity of light in vacuum) = 2.9979 × 108 ms−1
- μ = wavelength in μm
- T = temperature in K
Human skin emits infrared radiation mainly in the wavelength range of 2–20 μm with an average peak of 9–10 μm []. Based on Plank’s Law roughly 90% of the emitted infrared radiation in humans is of longer wavelength (8–15 μm).
Figure 1 gives an overview of the medical imaging modalities used within the electromagnetic spectrum.
Typical imaging modalities within the electromagnetic spectrum.
4. Infrared Radiation
Emissivity refers to an object’s ability to emit radiation [27]. Infrared cameras generate images based on the amount of heat dissipated at the surface by infrared radiation. The technology is a sophisticated way of receiving electromagnetic radiation and converting it into electrical signals. These signals are finally displayed in gray shades or colors which represents temperature values. Human heat energy is transferred to the environment via four mechanisms []:
- Conduction: the transfer of heat energy via tissue layer by contact between two bodies of different temperatures;
- Convection: the heat change between the skin and the surroundings; and
- Radiation: a transfer of heat that does not require a medium. The energy is transferred between two separate objects at different temperatures via electromagnetic waves (photons)
- Sweat Evaporation: which is the main mechanism for heat dissipation during exercise? The conversion of liquid into vapor allows the body to regulate its temperature. Evaporation results in a decrease of surface temperature.
The constructed thermogram yields a quantitative and qualitative temperature map of the surface temperature, which can be related to distinct pathological condition and blood flow.
Different to a single detector thermal camera, focal plane array detectors generate thermal images of high resolution without a mechanical scan mechanism. These cameras operate in the long wave infrared region (8–15 μm) with the advantage that they are less affected by sunlight compared to the shorter waves.
4.1. The 21st Century Technique
The medical usefulness of infrared thermography has been proven over the last several years but has largely been done without the advantage of 21st century techniques [29].
A new generation of high-resolution cameras has been developed, leading to improved diagnostic capability. Changes in the thermal pattern that may be very small but still meaningful can be properly assessed.
These technical enhancements have made infrared thermography into a reliable and powerful measurement tool [30]. It has opened opportunities for very precise measurements by imaging very subtle changes in skin surface temperature. Table 1 gives an overview of recent technical developments.
Table 1.
OLD TECHNIQUE | NEW TECHNIQUE |
---|---|
Liquid detector cooling | Uncooled camera technology |
Single element detector | Focal plane array detector |
Slow mechanical scan mechanism | Real time, high-speed imaging with multi elements arrays |
Low resolution camera | High-resolution camera |
Analogue conversion and computing | Digital conversion and computing, electronic transfer of images from camera to PC in real time |
No sufficient knowledge about standardization methods | Standardization protocols and recommendations for medical use |
Gray shade images | Color visible images |
Expensive, big in size, not mobile | Affordable, smaller and fully mobile |
Predominantly low sensitivity | Improved sensitivity (0.02 degrees celcius) |
Insufficient software and tools | User-friendly image processing software |
4.2. Recommended Requirements for Human Medicine
The thermal imaging group from the University of Glamorgan has recently published a battery of tests for checking the reliability of an infrared camera [23,31].
An infrared camera suitable for evaluating human skin profiles should have the following [31–33]:
- High Spatial resolution which reflects the separation between two nearby spots. A resolution of 320 (horizontal) × 240 (vertical) pixel is the minimum requirement. The spatial resolution is very dependent on image focusing.
- High Thermal resolution as an expression of sensitivity, defined as the minimum temperature difference that can be measured at two distinct spots.
- Medical CE certification is recommended: As soon as a temperature value in degree celcius is stated, the device is classified as a medical modality with a measuring function and should be signed by a specific CE approval.
- Narrow Calibration range accustomed to the human temperature range (i.e., 20–40 °C) assures more detailed temperature readings.
- Medical examination software including an export function, for medical analysis report and well-designed software tools for data analysis and image fusion (Figure 2).Process of image fusion. (a) Anatomical image; (b) Image fusion first step; (c) Image fusion second step; (d) Infrared Image.
In general, an area read-out of at least 8 × 8 pixels should be used instead of hot spot measurements [34]. According to Mayr [35] a line shaped and rectangular form (as seen above) is possible when assessing side-to-side differences. The upper and lower edge of the patellae as well as the tibial tuberosity can be clearly defined by image fusion and is therefore recommended for use as an anatomic marker system [].
5. Reliability Study
Reliable measurements have a substantial impact on the diagnosis and interpretation of pathophysiological abnormalities. Many investigations about reliability have focused on equipment and errors related to the physical principles of the technique [31,]. In addition to technical variations, biological changes such as the circadian rhythm may also contribute noise to the measurements [38].
The reproducibility of the thermal pattern is important if MIT is to be used as a screening tool for injuries. Selfe et al. [] conducted a study of inter-rater reliability and determined that MIT generated adequately reliable thermal patterns from the anterior knee.
The amount of heat emitted from the knee is a complex phenomenon that is influenced by many factors and comparing images over time requires good standardization methods and quality assurance []. We conducted a preliminary study to evaluate the day-to-day repeatability [40]. To guarantee reliable measurements, a standardized setup was used as shown in Figure 3.
Set up for measurement.
5.1. Methods of Reliability Study
Mean temperature readings of the anterior aspect of the knee of 15 subjects were analyzed. To eliminate inter-rater error, the same person carried out the measurements each time. The examination was conducted according to the “Glamorgan Protocol” which was established to ensure quality control when using MIT for medical applications [23].
To provide consistency for repeated measurements, anatomical landmarks were marked on the subject to delineate the region of interest for data capture.
5.2. Results
While high individual variations in knee temperature between subjects were noted, low variations between day-to-day measurements indicated the overall stable temperature of the knee. The one-way random intra-class correlation coefficient (ICC) indicated good intra-examiner reliability for absolute values of mean temperature for the right leg and moderately good reproducibility for the left leg (Table 2).
Table 2.
Intra-examiner reproducibility of mean knee temperature
Intra-examiner reliability of the mean Temperature (n = 15) | ||
---|---|---|
ICC | Rangea | |
Right leg | 0.85 | 0.61–0.94 |
Left leg | 0.75 | 0.41–0.90 |
In agreement with other studies, we concluded that MIT is a promising evaluation tool when administered under standardized conditions [1,–]. The results of these studies were recently published in the journal Thermology International and provide a more detailed description of methods [40].
6. Clinical Application in Alpine Skiing
Previous research has demonstrated that thermal images from the two sides of the body are usually symmetrical [42,43]. Any significant asymmetry of more than 0.7 °C can be defined as abnormal and may indicate a physiologic or anatomical variant in the loco-motor system. By comparing one side with the other, it may be possible to detect sub clinical problems before they are clinically relevant.
One of the most beneficial contributions of MIT to sports medicine may be in the field of preventive medicine. Turner et al. [] examined tendonitis in racehorses and thermographically detected hot spots two weeks before clinical evidence of swelling, pain and lameness. Early detection of abnormal changes in the tissues is important to counteract overuse injuries. The knee is exposed to a lot of physical stress during the alpine skiing competition season. The so-called “little traumatologies” are very frequent; therefore, their early detection is important []. However, it must be emphasized that the primary goal is to detect irregularities in the symmetry of temperature distribution rather than the measurement and comparison of absolute temperatures.
There are currently no quick screening tools that are sufficiently predictive of impending symptoms. To verify the thesis that MIT could predict symptoms, we conducted a pre-season measurement of 35 female and 52 male junior alpine ski racers. This study included likewise athletes who were in rehabilitation after traumatic and acute injuries.
6.1. Methods
Following an acclimatization period of 20 minutes, we recorded an image of the anterior/posterior and medial/lateral aspect of both knees with an infrared camera (TVS500EX). A fixed distance of 95 cm from the camera to the subject was used.
Data were stored and analyzed with the iREPORT 2007 software, provided by the GORATEC GmbH. All images were corrected using an emissivity factor of 0.98. Image fusion was used to identify the area of interest. The room temperature remained constant ranging from 21.5–22.3 °C. Equally the relative humidity showed stable values over time (35–38%).
Infrared images were taken twice to get pre- and postseason measurements. Thermographic evaluation was done according to the guidelines prepared by the medical members of the American Academy of Thermology (AAT) and the Glamorgan protocol [23], which incorporates the following seven aspects:
- Patient communication
- Patient preparation
- Patient assessment
- Examination guidelines
- Review of the imaging examination
- Presentation of the findings
- Exam time recommendation continuing professional education
An experienced team of sports physiotherapists conducted the musculoskeletal examination to obtain data about the functional aspects of the knees. Each subject had to fill in a questionnaire to get additional information about:
- Name, age, sex
- Sport history including information about training performed in the previous 7 days
- Health status
- Nutritional status
- Menstrual cycle
6.2. Case Studies
6.2.1. Overuse Injuries
A common problem in alpine skiing is the occurrence of overuse injuries such as patellae tendinopathy, which is characterized by swelling, pain and tenderness above the tibial tuberosity []. This regional problem becomes apparent in the form of a hyperthermic pattern, as can be seen in Figure 4 in which the right knee is affected. The preseason training program includes excessive jumps, leading to mechanical strain and overuse of the patella tendon.
Infrared image of the anterior aspect of the knees (Enthesopathy of the ligamentum patellae affects the right knee). The temperature scale applies for each infrared image below.
In this study, a total of seven athletes showed symptoms of regional overuse reactions. The symptomatic athletes had a mean side temperature differences of 1.4 °C (±0.58 °C). The normal temperature range of the eight non-injured athletes showed a side-to-side variation of 0.3 °C (±0.61 °C).
Four of the injured athletes reported pain, while the others were asymptomatic at that time. However, physical examination of the knee revealed that this hyperthermia was associated with a low threshold for pressure pain, as previously described in the literature [46].
Early detection and subsequent early therapy intervention program can reduce the severity of symptoms. Furthermore, the detection of at-risk athletes makes it possible to adjust their training program.
6.2.2. Traumatic Injuries
Epidemiological studies have shown a high incidence of serious knee injuries among alpine skiers, with the most common injury being the rupture of the anterior cruciate ligament (ACL) [,]. In Figure 5, the image on the left side was taken 6 weeks follow–ing an isolated ACL rupture of the right knee. The massive hyperthermia around the lower patellae represents the inflammation process, which is accompanied by swelling and pain. The image on the right side shows the same knee following 6 months of extensive rehabilitation program.
Infrared image of the anterior aspect of the knees (ACL rupture in the right knee).
A clear decline in swelling and inflammation can be seen. However, pain sensation is still present on the medial aspect of the right knee, as indicated by the hyperthermic area.
Severe alpine skiing accidents may result in serious injuries such as fractures. In Figure 6, the infrared image on the right side was taken 3 months after a combined fracture of the tibia and fibula with intramedulary nailing. This injury resulted in a clear demarcation and localization making it possible to define the extent of the high metabolic activity in structures involved.
Infrared image of the anterior aspect of the knees (fracture tibia and fibulae in the right knee).
Following treatment, no clear differences of the temperature distribution between the two sides could be noted. In conjunction with the clinical examination, the complete recovery was confirmed. However, a high temperature on the shank can be noted on both legs, possibility due to increased muscular activity. Follow up imaging is required for long-term evaluation.
The incidence of soft tissue injuries such as muscle strains is relatively small in alpine skiing []. However, these injuries are a strong risk factor for future strain injury to the same muscle. Full recovery needs to be assured and may be visualized threw thermal imaging.
It is very important to understand the pathophysiology, phases and time frame of normal tissue healing of traumatic injuries. Regular MIT measurements within the rehabilitation process provide information about the ongoing healing process and improve the therapist’s ability to create an adapted rehabilitation and treatment program. Infrared images may give full recovery information by indicating by low side-to-side differences and decreasing the likelihood of re-injury by returning to the sport too quickly.
These results are based on primary investigations and can be regarded as a first step to provide a scientific database for validating overuse and acute knee injuries when examined with MIT. Further research is intended to distinguish between normal and abnormal temperature patterns [49].
7. Limitations and Advantages of Infrared Imaging
The efficiency, safety and low cost of MIT make it an auxiliary tool in medical imaging and diagnostics [,50]. It can be applied without any objections because this non-invasive technique works without damaging radiation. It has the potential for performing in vivo diagnosis on tissues without the need of sample excision; hence, it can be regarded as a passive measurement [30]. Furthermore, the resulting real time information can be used as instant feedback for the patient or athlete. Innovative concepts such as dynamic thermal imaging will be applied to further explore skin thermal properties in response to stresses such as excessive jumping performance and training, as one important part of specific training in alpine skiing [].
Cutaneous temperature changes during exercise can now be detected by functional thermal imaging using state-of -the art infrared sensor arrays and may provide additional useful data [–].
However, infrared thermography becomes even more useful when its limitations are known. For future consideration, it is important to know that this can provide physiological information but cannot define aetiologies and local anatomy. The Individual variability combined with the complex character of thermoregulation limits the interpretation. The lack of specificity makes it necessary to combine these measurements with other, more structural modalities (X-ray, computed tomography), rather than using it as a replacement.
The biggest challenge is to combine the anatomical and physiological information given by the thermal pattern of the skin surface. The use of instrumented techniques to measure circulatory conditions must be considered.
Automated overlay of infrared and visual medical images as well as automated target recognition are also being actively studied [,57]. By applying these new techniques we may reduce operator dependence and enhance accuracy and objectivity.
8. Conclusions
Thermal imaging in medicine is not new, but early investigation with old and insufficient techniques has led to work with dubious results. Recent work with modern 21st century technology has demonstrated the value of MIT in medical application when used as an auxiliary tool. Knowledge about thermoregulation, anatomy, physiology, morphology and pathophysiological processes is important to counteract inaccurate diagnoses.
The aim of this technique is not to be a substitute for clinical examination but to enhance it. Further research and follow-up studies are warranted to create databases for clinical measurements and further determine its viability in real-world medical settings. Empirical evidence of correlation between pathology and infrared imaging is essential to further predict the value of MIR. It should be used as a multidisciplinary assessment tool by experts from different fields.
Based on the advantages of MIT as a non-invasive, non-radiating, low cost first-line detection modality, it should be applied in the field of sports medicine as a pre-scan team assessment tool. The extension of sport specific databases may further contribute to the detection of high risk athletes and help them to start early intervention.
Table 3.
Temperature readings (°C) of the area above the tibial tuberosity (n = 7).
Affected knee | Non-affected knee | Temperature differences | |
---|---|---|---|
Mean | 32.8 (± 0.48) | 31.1 (± 0.32) | 1.4 (± 0.58) |
Minimum | 31.4 (± 0.43) | 30.3 (± 0.41) | 0.8 (± 0.31) |
Maximum | 33.4 (± 0.39) | 32.1 (± 0.60) | 1.3 (± 0.64) |
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Articles from Sensors (Basel, Switzerland) are provided here courtesy of Multidisciplinary Digital Publishing Institute (MDPI)
Published online 2015 Oct 26. doi: 10.5535/arm.2015.39.5.696
PMID: 26605167
This article has been cited by other articles in PMC.
Abstract
Objective
To investigate changes in the core temperature and body surface temperature in patients with incomplete spinal cord injuries (SCI). In incomplete SCI, the temperature change is difficult to see compared with complete spinal cord injuries. The goal of this study was to better understand thermal regulation in patients with incomplete SCI.
Methods
Fifty-six SCI patients were enrolled, and the control group consisted of 20 healthy persons. The spinal cord injuries were classified according to International Standards for Neurological Classification of Spinal Cord Injury. The patients were classified into two groups: upper (neurological injury level T6 or above) and lower (neurological injury level T7 or below) SCIs. Body core temperature was measured using an oral thermometer, and body surface temperature was measured using digital infrared thermographic imaging.
Results
Twenty-nine patients had upper spinal cord injuries, 27 patients had lower SCIs, and 20 persons served as the normal healthy persons. Comparing the skin temperatures of the three groups, the temperatures at the lower abdomen, anterior thigh and anterior tibia in the patients with upper SCIs were lower than those of the normal healthy persons and the patients with lower SCIs. No significant temperature differences were observed between the normal healthy persons and the patients with lower SCIs.
Conclusion
In our study, we found thermal dysregulation in patients with incomplete SCI. In particular, body surface temperature regulation was worse in upper SCIs than in lower injuries. Moreover, cord injury severity affected body surface temperature regulation in SCI patients.
Keywords: Spinal cord injuries, Body temperature regulation, Body temperature, Skin temperature, Thermography
INTRODUCTION
Autonomic dysfunction accompanied by spinal cord injury (SCI) appears in the form of diverse symptoms such as neurogenic shock, arrhythmia, orthostatic hypotension, autonomic dysreflexia, and thermoregulatory dysfunction []. Because autonomic dysfunction might threaten life in the early stage of SCI, it needs to be evaluated accurately. Temperature, one of the evaluation indices of autonomic dysfunction, maintains homeostasis against external environment changes and is relatively easy to measure. Thus, temperature can be used as a useful tool for evaluating autonomic nervous system functioning in the early stage of spinal cord injury. Body surface temperature is also known to be regulated by the autonomic nervous system and to have complex interactions with the physical conditions of the surrounding environment, skin fat and dermis thickness, and internal heat conduction and convection [,]. Regarding body temperature maintenance, it has been reported that there is a complex interaction between core temperature receptors and peripheral skin temperature receptors []. Therefore, in assessing thermoregulatory function in SCI patients, it would be helpful to evaluate not only core temperature but also body surface temperature at the same time. Recently, digital infrared thermographic imaging (DITI) has been used widely to measure body surface temperature. DITI can detect infrared radiation emitted from the body surface for digitization and visualization [,], and the sympathetic nervous system can be quantitatively evaluated in a relatively easy and quick manner.
In the previous studies on changes in core temperature and body surface temperature of SCI patients, these patients were reported to show declines in core temperature and trunk temperature depending on the level of injury. Most studies have investigated complete SCI, and as such, there are insufficient studies about patients with incomplete SCI [,11,]. In these patients, the degree of autonomic nervous system dysfunction is not severe compared with patients with complete SCI, which might make it difficult to accurately evaluate the dysfunction [,13]. This study aims to measure core temperature and body surface temperature in normal healthy persons and in patients with incomplete SCI for comparative analysis by location and duration of injury and severity. This is intended to help evaluate thermoregulatory dysfunction in incomplete SCI patients, which has not been studied sufficiently to date.
MATERIALS AND METHODS
Subject
This study enrolled SCI patients with body mass index (BMI) values of 22.0-25.0 kg/m2 who had been hospitalized in the department of rehabilitation medicine of our hospital from January 1, 2014 to December 31, 2014. Among 64 SCI patients, 8 were excluded with autonomic function disorder, peripheral vascular disorder, peripheral nerve disorder, muscular skeletal disease, and skin lesion. Among the remaining 56 patients, there were 49 men and 7 women with average age of 52.5±12.6 years old. Among SCI patients who consented to DITI study, 29 patients with neurological injury level at T6 or above and 27 with injury level at T7 or below participated in this study according to the International Standards for Neurological Classification of Spinal Cord Injury classification. The control group consisted of 20 healthy adults.
Method
Measuring core temperature
Oral thermometers are widely used to measure core temperature. In this study, an oral thermometer was placed under the tongue for approximately 5 minutes for measurement. Measurements were taken twice so that the median value could be used.
Measuring body surface temperature
DITI (Iris-XP; Medicore Co. Ltd., Seoul, Korea) was used to measure body surface temperature. The DITI device consists of an infrared camera, a computer, and an LCD monitor. The infrared camera lens measures infrared radiation that is emitted from the body's surface to show temperature differences by color. The temperature of the infrared thermographic imaging room was maintained at 19℃-20℃, and the humidity was approximately 60%. Light and heat were blocked and indoor airflow was maintained constantly. Before the thermographic imaging was measured, the standard guideline of the American Academy of Thermology that was announced in 1987 was followed [14]. Patients were asked to stop taking medications that could have affected the autonomic nervous system at least 3 days prior to examination. One day before examination, patients were also asked to refrain from physical therapy, thermotherapy, and electrophysiologic study. To exclude the effect of the circadian rhythm of body temperature, measurements were taken between 8 AM and 9 AM in a fasting state. Subjects were undressed and acclimated to the examination room temperature for 20 minutes. Then, DITI was taken at approximately 1.5 m away from the camera. Body surface temperature was measured at the anterior thigh, anterior tibia and lower abdomen. Average value was used after 4 measurements were taken by a single examiner, and median value was used after both sides were measured.
Statistical analysis
SPSS ver. 18.0 for Windows (SPSS Inc., Chicago, IL, USA) was used for the statistical analysis. One-way analysis of variance (ANOVA) was used to compare BMI and age among the 3 groups. The Kruskal-Wallis test was used to compare the anterior thigh, anterior tibia, and lower abdomen temperatures in each of the 3 groups. Then, for the post hoc test, the Mann-Whitney test with Bonferroni correction was used to test for statistical significance. To compare differences between the SCI group at T6 or above and the group at T7 or below by injury severity and injury duration, the Mann-Whitney test was used for statistical significance, and significance was set at below 0.05. With the Mann-Whitney test with Bonferroni correction, p-value was set below 0.017.
RESULTS
Demographic data
Among the 29 SCI patients who were at T6 or above, average age was 54.9±10.0 years and average injury duration was 283 days. The number of acute SCI patients of less than 7 months' duration was 16, and that of chronic patients of more than 6 months was 13. Among the 27 SCI patients who were at T7 or below, average age was 50.5±12.0 years and average injury duration was 354 days. The number of acute SCI patients of less than 7 months' duration was 17, and that of chronic patients of more than 6 months was 10. Among the 20 healthy adults in the control group, average age was 48.1±4.8 years. Among the SCI patients at T6 or above, all 29 patients had cervical injuries; thoracic injury patients were not recruited. Among the SCI patients at T7 or below, there were 21 thoracic injury patients and 6 lumbar injury patients. There were no statistically significant differences among the 3 groups in terms of age or BMI (Table 1).
Table 1
Values are presented as number or mean±standard deviation.
SCI, spinal cord injury; Upper SCI, neurological injury level is T6 or above; Lower SCI, neurological injury level is T7 or below; AIS, American Spinal Injury Association impairment scale; BMI, body mass index.
Body surface temperature distribution by group
Core temperature and body surface temperature were compared among the healthy adults, the SCI patients at T6 or above and the SCI patients at T7 or below (Table 2). The measurement results for the healthy adults were as follows: core temperature 36.6℃±0.2℃; body surface temperature of anterior thigh 30.0℃±0.5℃; body surface temperature of anterior tibia 30.0℃±0.6℃; and body surface temperature of anterior lower abdomen 29.9℃±0.4℃. The differences between maximum and minimum temperature at each area were 0.21℃±0.17℃ at anterior thigh, 0.21℃±0.15℃ at anterior tibia, and 0.24℃±0.13℃ at lower abdomen. The measurement results for the SCI patients at T6 or above were as follows: core temperature 36.4℃±0.2℃; body surface temperature of anterior thigh 28.8℃±0.9℃; body surface temperature of anterior tibia 28.5℃±0.℃; and body surface temperature of lower abdomen 28.5℃±0.7℃. The differences between maximum and minimum temperature at each area were 0.21℃±0.11℃ at anterior thigh, 0.26℃±0.15℃ at anterior tibia, and 0.20℃±0.16℃ at lower abdomen. The measurement results for the SCI patients at T7 or below were as follows: core temperature 36.5℃±0.4℃; body surface temperature of anterior thigh 29.8℃±0.9℃; body surface temperature of anterior tibia 29.7℃±0.7℃; and body surface temperature of lower abdomen 29.6℃±0.6℃. The differences between maximum and minimum temperature at each area were 0.23℃±0.13℃ at anterior thigh, 0.25℃±0.16℃ at anterior tibia, and 0.21℃±0.16℃ at lower abdomen. There were no statistically significant differences in the comparisons of core temperature among the 3 groups.
Table 2
Comparison of body core temperature and skin temperature among the three groups
SCI, spinal cord injury; Upper SCI, neurological injury level is T6 or above; Lower SCI, neurological injury level is T7 or below.
a)Statistically significant (p<0.017) difference between upper SCI and lower SCI by Mann-Whitney test with Bonferroni correction.
b)Statistically significant (p<0.017) differences between upper SCI and control group by Mann-Whitney test with Bonferroni correction.
*p<0.05 by Kruskal-Wallis test.
Comparing body surface temperatures at the anterior thigh, there was a difference of 1.2℃ on average between the healthy adults and the SCI patients at T6 or above, a statistically significant difference (p<0.017). There was a difference of 0.2℃ on average between the healthy adults and the SCI patients at T7 or below, which was not statistically significant. There was a difference of 1.0℃ on average between the SCI patients at T6 or above and those at T7 or below, which was statistically significant (p<0.017).
Comparing body surface temperatures at the anterior tibia, there was a difference of 1.5℃ on average between the healthy adults and the SCI patients at T6 or above, which was statistically significant (p<0.017). There was a difference of 0.3℃ on average between the healthy adults and the SCI patients at T7 or below, which was not statistically significant. There was a difference of 1.3℃ on average between the SCI patients at T6 or above and those at T7 or below, which was statistically significant (p<0.017).
Comparing body surface temperatures at the lower abdomen, there was a difference of 1.4℃ on average between the healthy adults and the SCI patients at T6 or above, which was statistically significant (p<0.017). There was a difference of 0.3℃ on average between the healthy adults and the SCI patients at T7 or below, which was not statistically significant. There was a difference of 1.1℃ on average between the SCI patients at T6 or above and those at T7 or below, which was statistically significant (p<0.017).
In the SCI T6 and SCI T7 patients, core temperature and body surface temperature were compared between the acute SCI patients of less than 7 months and the chronic SCI patients of more than 6 months (Table 3). The differences were not significant in the core and body surface temperatures of the anterior thigh, anterior tibia, and lower abdomen.
Table 3
Comparison of body core temperature and skin temperature between acute phase and chronic phase SCI
Values are presented as mean±standard deviation.
SCI, spinal cord injury; Upper SCI, neurological injury level is T6 or above; Lower SCI, neurological injury level is T7 or below.
In the SCI patients at T6 or above and those at T7 or below, core and surface temperatures were compared between American Spinal Injury Association impairment scale (AIS) B and C and AIS D patients (Table 4). The measurement results for AIS B and C patients among the SCI patients at T6 or above were as follows: core temperature 36.5℃±0.2℃; body surface temperature of anterior thigh 28.2℃±1.1℃; body surface temperature of anterior tibia 28.0℃±0.6℃; and body surface temperature of lower abdomen 27.8℃±0.6℃. The corresponding measurement results in the AIS D group were as follows: core temperature 36.4℃±0.3℃; body surface temperature of anterior thigh 28.9℃±0.8℃; body surface temperature of anterior tibia 28.8℃±0.8℃; and body surface temperature of lower abdomen 28.7℃±0.9℃. The results showed that the body surface temperatures of the anterior thigh, anterior tibia, and lower abdomen were approximately 0.8℃ higher in the AIS D group, a statistically significant difference (p<0.05). The measurement results for the AIS B and C group among SCI patients at T7 or below were as follows: core temperature 36.5℃±0.2℃; body surface temperature of anterior thigh 29.0℃±0.8℃; body surface temperature of anterior tibia 29.2℃±0.7℃; and body surface temperature of lower abdomen 29.3℃±0.5℃. The corresponding measurement results in the AIS D group was as follows: core temperature 36.5℃±0.2℃; body surface temperature of anterior thigh 29.7℃±0.9℃; body surface temperature of anterior tibia 29.8℃±0.6℃; and body surface temperature of lower abdomen 29.9℃±0.6℃. Between the two groups, the body surface temperatures of the anterior thigh, anterior tibia, and lower abdomen approximately 0.6℃ higher in the AIS D group, a statistically significant difference (p<0.05).
Table 4
Comparison of body core temperature and skin temperature between AIS B and C and AIS D in SCI
Values are presented as mean±standard deviation.
SCI, spinal cord injury; Upper SCI, neurological injury level is T6 or above; Lower SCI, neurological injury level is T7 or below; AIS, American Spinal Injury Association impairment scale.
a)Statistically significant (p<0.05) difference between AIS B, C and AIS D in upper SCI by Mann-Whitney test.
b)Statistically significant (p<0.05) difference between AIS B, C and AIS D in lower SCI by Mann-Whitney test.
DISCUSSION
The human body's temperature is maintained constantly by a sophisticated thermoregulatory center in the hypothalamus. Heat and cold signals are carried by the afferent nerve to the hypothalamus, which then integrates this information to regulate thermogenesis by activating or inhibiting the sympathetic nervous system [15]. Thermal regulation is impaired in patients with SCI. As a result, they cannot appropriately respond to the changing temperatures of their surrounding environments. This phenomenon is called poikilothermia [13]. Constant exposure to low or high temperatures can cause bleeding, metabolic acidosis, arrhythmia, decline in cardiac contractility, and exercise-induced hyperthermia [,]. It was reported in preceding studies that this phenomenon could happen frequently among patients with SCI, especially in those with complete lesion at T6 or above [13]. This is attributable to the loss of supraspinal control regulated by the hypothalamus and to damage to the afferent and efferent pathways of the sympathetic nervous system. All of these lead to dysregulation in vasomotor tone, skeletal muscle shivering and sweating dysfunction [22].
Skin plays an important role in regulating body temperature as a dynamic membrane that regulates interactions between surrounding environments and the human body []. Body surface temperature is affected by diverse factors but is mainly regulated by the sympathetic nervous system. It is known that there is a complex interaction among core temperature, body surface blood flow, physical conditions of the surrounding environment, skin fat and dermal thickness, internal heat conduction and convection, and body temperature circadian rhythm [,]. To measure body surface temperature, contact thermography and DITI can be used. DITI is being used widely because it is convenient and can measure changing body temperatures as accurately as contact thermography [,]. Chun et al. [28] reported that absolute temperature measured through DITI had low diagnostic efficacy because of fluctuation. However, in the study of Chun et al. [28], the severe temperature changes and low diagnostic efficacy are assumed to have happened because physical conditions such as the study subjects' circadian rhythms and BMIs were not considered. In this study, to exclude factors that might have affected body surface temperature changes, examinations were conducted between 8 AM and 9 AM, and physical environmental conditions were maintained constantly. In particular, to exclude internal factors, BMI was considered in selecting the SCI patient group and the healthy adults. In this study, the differences between each individual's minimum and maximum temperature were found to be more stable than were the findings from other studies including that of Chun et al. [28].
Downey et al. [] confirmed the existence of central thermoreceptors and peripheral cold receptors in the skin surface regarding body temperature regulation. With SCI patients at T6 or above, body temperature is mainly regulated by central thermoreceptors. Meanwhile, in SCI patients at T7 or below, both core temperature and body surface temperature receptors have an effect. It has been reported that this caused more severe dysfunction in body temperature regulation against external temperature change among SCI patients at T6 or above. In this study, SCI patients at both T6 or above and T7 or below were exposed to an environment of approximately 20℃. In the process, this study referred to preceding studies that used DITI to investigate both healthy people and SCI patients [11,28]. We observed core temperature decline among healthy adults, SCI patients at T6 or above or SCI patients at T7 or below. However, body surface temperature in SCI patients at T6 or above was lower than that in SCI patients at T7 or below and in healthy adults. This confirmed that dysfunction in body surface temperature regulation was more severe among SCI patients at T6 or above, which was similar to the results in Downey et al. [].
It is known that more severe SCI causes more severe dysfunction in body temperature regulation [13]. Accordingly, this study compared core and body surface temperatures based on the severity of SCI. Because of the limited number of recruited subjects, this study compared AIS B and C patients with AIS D patients (Table 4). Among SCI patients at T6 or above and those at T7 or below, core temperature did not show a significant difference between AIS B and C patients and AIS D patients. However, in terms of body surface temperature, a significant difference was observed between the AIS B and C and AIS D groups (p<0.05). This confirmed body surface temperature regulation dysfunction among AIS B and C patients compared with AIS D patients with relatively low degree of injury among incomplete SCI patients.
Some previous studies have investigated changes in core and body surface temperatures among SCI patients. Khan et al. [] studied hypothermia frequency by measuring body temperature in 50 patients who had experienced their SCIs more than 5 years prior to the study. Body temperature was measured 867 times, and roughly 63% of participants showed subnormal temperatures (35℃-36.5℃); roughly 3% showed hypothermia (<35℃). In the present study, body temperature was measured 26 times among 13 chronic SCI patients who were at T6 or above. The results showed that 57% demonstrated subnormal temperatures and that hypothermia was not observed. In the study by Khan et al. [], most of the 50 patients corresponded to AIS grade A and the study subjects were in the chronic phase of their injuries, that is, SCI of more than 5 years' duration. In this study, most of the cervical injury patients corresponded to AIS grade D, and the average injury duration among SCI patients at T6 or above was 283±147 days, which was shorter and presumably led to different study results.
Claus-Walker et al. [] reported that cold stimuli among complete SCI patients could cause hypothermia. It has also been reported that the longer the duration of SCI, the more body temperature regulation function could decline. Studies reported that most functions were recovered in the first 6 months after SCI [,]. In this study, we measured core body temperature and body surface temperature in incomplete SCI patients to compare thermal regulation function by injury duration. SCI patients at T6 or above and those at T7 or below were divided into acute and chronic patients, with the cut-off at 6 months. There were no significant temperature differences by injury duration in any group in core or body surface temperature at the lower abdomen, anterior thigh, or anterior tibia. Body temperature regulation was maintained relatively constantly regardless of injury duration among incomplete SCI patients compared with complete SCI patients. Claus-walker et al. [] studied complete SCI patients, and average injury duration among them was 101±45 months. However, we studied incomplete SCI patients, and the average injury duration of chronic SCI patients was 43.8±40.0 months, which presumably is the reason for the different study results from those of Clauswalker.
Another factor that might affect body surface temperature is pain. No correlation between pain and body surface temperature changes has been clearly identified yet []. However, many preceding reports have described some relationship between skin temperature changes by DITI and pain from radiculopathy or nerve entrapment syndrome [,35]. In particular, body temperature change according to central pain is still controversial in many studies [,11,]. Park et al. [11], on central pain after SCI, reported that the complete SCI patient group with central pain showed significantly lower body surface temperatures as measured through DITI than did the patient group without central pain. Sherman et al. [] reported that body surface temperature dropped at the skin level below the cord injury and that body surface temperature was higher in the area with central pain. In this study, 26 out of 29 SCI patients at T6 or above complained of central pain and 25 out of 27 SCI patients at T7 or below did so. Because most patients complained of central pain, it was impossible to conduct statistical verification of body surface temperature based on the presence of central pain. In the future, more advanced studies need to be carried out by recruiting patient groups based on the presence of central pain.
With regard to the limitations of this study, the patient group of T6 or above were all cervical injury patients because thoracic injury patients were not recruited. Among the lower cord injury patients, thoracic cord injuries outnumbered lumbar injuries, which made it impossible to conduct a comparative analysis by level of injury. Body surface temperature was measured only at the lower limbs and lower abdomen, not at the posterior surfaces of the lower limbs. Separately, the recruited women's menstrual cycles were not considered. However, because women accounted for less than 15% in each group, menstrual cycle are assumed to have had little effect. Another limitation is that no comparative analysis was conducted based on the presence of central pain because most patients complained of central pain. In the future, these limitations need to be considered in order to conduct more studies on core temperature and body surface temperature in spinal cord injury patients.
In SCI patients and healthy adults, core temperature was measured along with body surface temperature at the anterior thigh, anterior tibia, and lower abdomen using DITI. The aim was to confirm dysfunction in body surface temperature regulation among incomplete SCI patients. The body surface temperature regulation dysfunction was especially severe among SCI patients at T6 or above compared with patients at T7 or below. It was also confirmed that the more severe the cord injury, the greater the dysfunction in body surface temperature regulation. Because this study enrolled incomplete SCI patients, declining core temperature was not observed compared with preceding studies on complete SCI patients. However, we observed that body surface temperature in SCI patients was lower than that among healthy adults. Body surface temperature declined significantly, especially among patients at SCI T6 or above compared with healthy adults and the SCI patient group at T7 or below.
Footnotes
CONFLICT OF INTEREST: No potential conflict of interest relevant to this article was reported.
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Rehabilitation Medicine And Thermography Pdf
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