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Skin thermometry: new concepts*
(Portuguese PDF version)

Marcos Leal Brioschi¹, José Fernando Macedo², Rodrigo de Almeida Coelho Macedo³

1. Graduate student, Clinical Surgery, Universidade Federal do Paraná; Professor, Pontifícia Universidade Católica do Paraná; Member of the American Association of Thermology.
2. PhD; Member of the Brazilian Society of Angiology and Vascular Surgery; Member of the Brazilian School of Surgeons.
3. Undergraduate student, School of Medicine, Pontifícia Universidade Católica do Paraná.

*Study carried out by the Research Group in Infrared Imaging (Grupo de Pesquisa em Imagem Infravermelha) - PUCPR/CNPq

Correspondence:
Dr. Marcos Leal Brioschi
Rua da Paz, 195/115
CEP 80.060-160 - Curitiba - PR
E-mail: mbrioschi@hotmail.com

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ABSTRACT

The article approaches the use of a new diagnostic method for the objective assessment of functional disorders in patients with vascular diseases. This method, also known as high-sensitivity infrared skin thermometry, does not require any physical contact with the patient, is noninvasive and does not include a contrast medium. The authors describe the examination method, the necessary equipment, and the qualitative and quantitative evaluation parameters. The results of the examination allow the identification of vascular disorders, as well as of problems with the neuronal and musculoskeletal systems, inflammatory processes, dermatological, endocrine and oncological conditions. It permits us to assess the clinical prognosis and, consequently, solve medical problems more objectively.

Key-words: diagnosis, thermography, vascular diseases
Palavras-chave: diagnóstico, termografia, doenças vasculares.

J Vasc Br 2003;2(2):151-60

Maintenance of body temperature in humans is a complicated task. Man is homeothermic and produces heat that, in its turn, should be lost to the environment. The skin is the interface between heat production and the environment. So, it is constantly adjusted to balance the external and internal conditions and offset the body's physiological requirements. Sympathetic motor fibers control cutaneous microcirculation by way of vasoconstriction or vasodilation, causing lesser or greater irrigation of the skin. This control of heat transfer through the skin is defined as thermoregulation and depends upon the control of the autonomic nervous system.

Ischemic tissues often show decreased temperature and by feeling the back of the hand it is possible to notice some cooling if compared to the contralateral side.¹ Unfortunately, human beings only distinguish temperature changes that are on average greater than 2 ºC with this semiological technique.²

Infrared thermometry is the most efficient method currently available for studying the distribution of skin surface temperature. Skin thermometry is a diagnostic method that assesses cutaneous microcirculation and that also assesses, albeit indirectly, the sympathetic autonomic nervous system narrowly related to the skin. By measuring temperature changes caused by greater or lesser irrigation of a microvascular region, this technique allows perceiving tenths of centigrade degrees per squared millimeters of tissue area.²

Developed in the 1960s, telethermography or simply thermography, is a new noninvasive diagnostic method, which requires no contrast medium and is totally painless. In the 1980s, despite highly suggestive reports, low-resolution and low-sensitivity images were still obtained.^3-10 In our setting, the studies by Montoro & Barbosa,¹¹ Grosshans et al.,¹² Alves et al.¹³ and Elpo et al.¹⁴ are of note.

At the end of the 1990s, high-sensitivity infrared sensors were developed. The decisive factor was a sensitivity of up to 0.02 ºC and a detection in the long wavelength infrared spectrum (7.5 - 13 µm), obtained by supersensors known as FPA (focal plane array) of the QWIP (quantum well infrared photodetector) type.^9,10,15,16

Skin thermometry has become a diagnostic method that detects, records and produces infrared images (thermograms), reflecting the microcirculatory dynamics of patients' skin surface in real time. The procedure uses a mechanical system that positions the sensor close to the patient, in addition to computers that graphically represent the thermal patterns of human skin qualitatively and quantitatively, with high resolution and high sensitivity. These patterns, invisible to the naked eye and imperceptible to touch, are assessed as to their shape, distribution, symmetry with the opposite side and dynamic response to thermal and mechanical stimuli.¹⁷

VASCULAR DISEASES

Infrared thermometry may be safely indicated in all kinds of vascular diseases. Researchers admit that patients with pain in the extremities and with subjective temperature changes should be submitted to thermography.¹⁸ The information provided by skin thermometry is valuable to the diagnosis of peripheral vascular disorders caused by atherosclerosis, collagen diseases, Raynaud's syndrome, reflex sympathetic dysfunction and other causes. In some conditions, changes are quite specific, such as femoral artery occlusion, whose cause is detectable by the analysis of the thermal profile that is altered by collateral circulation around the knee.¹⁹

The use of thermography has significantly increased in the postoperative follow-up of patients submitted to vascular grafts. As this exam is harmless and noninvasive, it may be easily repeated.²⁰ Pharmacologically, thermography has been used to test and measure the vasomotor effects of drugs.²¹

Several studies show that it can also be used to determine the amputation level for ischemic limbs (Figure 1).^22,23

Figure 1 - Assessment of microcirculatory involvement and determination of amputation level through skin thermometry.

VARICOSE VEINS

Schalin²⁴ preoperatively located varicosities that corresponded to hot spots in thermometry. During surgery, this author microscopically observed that these spots were arteriovenous communications that ranged from 0.1 to 2 mm in diameter.

Funke et al.²⁵ and Wojciechowski et al.²⁶ studied patients with deep venous insufficiency through thermometry. Thermometry showed high sensitivity in detecting incompetent perforating veins comparatively to venography.

Kosichkin et al.²⁷ used thermometry to objectively assess the extent of functional alterations in patients with varicose veins of the lower extremities. The exam results allowed determining the extent of venous insufficiency precisely, appraising the valvar conditions of the veins, assessing the compensation possibilities of the vessel wall and the clinical prognosis, in addition to objectively estimating the work capacity of patients.

Reinharez,²⁸ Belcaro et al.²⁹ and Belcaro³⁰ assessed the treatment of thrombophlebitis and superficial vein thrombosis by means of thermometry. After using defibrotide and antithrombotic/profibrinolytic drugs or after the administration of low-dose subcutaneous heparin for three weeks, they observed thermal reduction of thrombosis.

Deep vein thrombosis

There is some stark evidence in favor of thermography when it comes to early detection of deep vein thrombosis.^19,31-39 Several unnecessary venographies can be avoided if they are only requested when thermography yields positive results.^40-42 Neither ultrasonography nor plethysmography can detect below-knee thrombi with such accuracy. Although pulmonary embolism is more frequently associated with above-knee thrombi, a considerable number of thrombi originate in the legs and subsequently migrate to the thighs. Thermography can diagnose thrombi above and below the knees, thus warning against possible pulmonary embolism, even if it is not so severe.

The diagnosis of deep vein thrombosis and the follow-up of treatment for this pathology are important indications of thermography. Lapayowker⁴³ showed that thermography is more sensitive and elucidative than venography under these circumstances. The diagnosis of calf pain still remains frustrating, especially in postoperative patients, but also in pregnant women who use oral contraceptives. In these cases, thermographic investigation is simple and brings noninvasive information.

Diabetic microangiopathy

Zykova & Popov⁴⁴ studied patients with different severity levels and duration of diabetes mellitus (DM). The authors spotted an image with thermal reduction that characteristically indicates amputation of feet and hands in cases of peripheral microangiopathy. In atherosclerotic arterial diseases, a more typical thermal asymmetry was observed. The authors used nitroglycerine to distinguish between organic and functional vascular lesions and to assess the compensation or not of peripheral circulation.

Many authors recommend the use of infrared thermometry for the assessment of sympathetic autonomic neuropathy.^45-49 After studying 62 DM patients, Fushimi et al.⁴⁵ used thermometry and observed absence of vasodilator activity in one of the legs after immersing the other leg in warm water. Thermal reduction was related to the duration of diabetes mellitus and to poor control of blood sugar levels. Thermography was largely related to microangiopathy and to the speed of motor nerve conduction and R-R interval on electroneuromyography. Musaev et al.⁵⁰ noted that naphthalan therapy was efficient in improving diabetic microangiopathy, by using thermometry to determine the prognosis of the disease.

Stess et al.,⁵¹ Chan et al.,⁵² and Armstrong et al.⁵³ used thermometry to predict plantar ulcers in diabetic peripheral neuropathy. Patients with high plantar temperature, especially in the metatarsal and calcaneal region, were at higher risk for foot ulcers. Low plantar temperatures in neuropathic feet were markers of ischemic peripheral vascular disease.

HEAD AND NECK VASCULARIZATION

Several authors advocate thermography for the diagnosis of extracranial carotid stenosis,⁵⁴ migraines and cluster headaches.^55,56

Another indication of infrared skin thermometry is in the examination of patients that are prone to these disorders due to atherosclerosis or hypertension. Unilateral periocular and supraorbital cooling, especially after the compression of the superficial temporal artery, is a sign of internal carotid insufficiency, which should be confirmed by angiography. This indication is especially important in the prevention of possible intraoperative ischemia during endarterectomies. Brain surgeons also admit that thermography is ideal for the follow-up of patients in the postoperative period, since it is a noninvasive technique. It may be repeated as often as necessary with no risk or discomfort to the patient.⁵⁴

CARDIOVASCULAR SURGERY

Infrared thermometry can be used intraoperatively during heart surgeries.^17,57,58 After the end of the distal anastomosis of the aortocoronary bypass, the perfusion of the venous graft reveals the heart area that is being actually supplied, what the blood flow is like and whether stenosis is present (Figure 2). Intraoperative infrared thermometry of the myocardium provides essential information for a successful surgery; in addition, this technique is not invasive and can be easily applied. The same principle can be adopted in surgeries of vascular limbs for assessment of muscular and cutaneous perfusion.²⁰

Figure 2 - Thermal coronary angiography showing perfusion of the anterior descending coronary artery and heart muscle.

NEUROLOGICAL DISORDERS

Sympathetic motor fibers control cutaneous microcirculation through vasoconstriction or vasodilation. A sensitive innervation site corresponds to a microvascular region, as sympathetic fibers follow sensitive fibers along the same nerve.^8,10,59-62 This allows us to divide the hand into sensitive innervation sites, which correspond to microvascular regions.

The extension comprised by each of the nerves defines a microvascular innervation site (Figure 3). Therefore, any nervous disorder alters the microvascular tone of the region corresponding to the sensitive innervation site.^{2,4,8,10,63-65}

Figure 3 - Neurovascular regions of the anterior (left) and posterior (right) sides of the body.

Adapted from Latarget⁶¹.

According to the literature,^2,8,10,63-65 the human body exhibits clear thermal symmetry after the proper preparation of the patient, whose subject areas are submitted to a constant room temperature^5,66 (Figure 4).

Figure 4 - High-sensitivity infrared thermometry. Normal dorsum. Observe the symmetry between the sides of the body.

When any asymmetry with the corresponding contralateral region exists, it is possible to diagnose neurovascular disorders. For this reason, an internationally standardized thermometric assessment is performed by comparing the corresponding sides of the human body,^2,8,10,63-65 while in traditional semiology, the assessment is carried out by the comparison of the opposite sides of the body with the back of the hands.

It should be underscored that the asymmetric image of a region does not necessarily mean local lesion of the cutaneous nerve. If more asymmetric areas exist, they can be related to larger involvement, corresponding to the dermatome of a spinal nerve.⁶⁴ The involvement of several regions, for instance, innervation sites that have L5 fibers (superficial fibular, common fibular, and anterior femoral cutaneous nerves), suggest L5 spinal nerve injury. Thus, the diagnosis based upon a single asymmetric region is not valid if the whole extension of the dermatome corresponding to that region is not assessed, that is, starting from the dermatome in the spinal column to the most distal portion, and comparing it with the respective side of the body.^3,6,64,67-69

In an examination of a lower limb, for example, 36 neurovascular regions are assessed (Table 1). In this case, it includes the whole limb, from the lumbosacral region to the most distal portion of the extremity, where many neuromuscular disorders originate. This examination should also include the contralateral limb, due to the principle of neurovascular symmetry between the sides of the body, as mentioned above. Only then it is possible to make the diagnosis, evaluate the severity and make the proper prognosis of the injury.^2,8,10,63-66

Table 1 - Neurovascular regions of the human body

Facial (head/neck)	Cervical (upper limbs)	Thoracic (abdomen)	Lumbosacral (lower limbs)
Ophthalmic nerve Maxillary nerve Mandibular nerve Great auricular nerve Great occipital nerve Small occipital nerve Cervical cutaneous nerve Transverse cervical nerve Lateral supraclavicular nerves Intermediate supraclavicular nerves Medial supraclavicular nerves Dorsal rami of cervical nerves Transverse cervical nerve Lateral supraclavicular nerve	Dorsal rami of cervical nerves Transverse cervical nerve Lateral supraclavicular nerves Intermediate supraclavicular nerves Medial supraclavicular nerves Dorsal rami of thoracic nerves Axillary nerve Intercostobrachial nerve Medial brachial cutaneous nerve Posterior brachial cutaneous nerve Medial antebrachial cutaneous nerve Posterior antebrachial cutaneous nerve Lateral antebrachial cutaneous nerve Superficial branch of radial nerve Median nerve Ulnar nerve Radial nerve	Lateral cutaneous branches from T1 to T12 Medial cutaneous branches from T1 to T12 Dorsal rami from T1 to T12	Dorsal rami of lumbar nerves Dorsal rami of sacral nerves Coccygeal nerves Iliohypogastric nerve Ilioinguinal nerve Genitofemoral nerve Posterior femoral cutaneous nerve Anterior femoral cutaneous nerve Lateral femoral cutaneous nerve Obturator nerve Common fibular nerve Superficial fibular nerve Deep fibular nerve Sural nerve Saphenous nerve Medial plantar nerve Lateral plantar nerve

 

Disorders of one or more regions may indicate an inflammatory process,^16,70 stress fractures,^71,72 chondromalacia,⁷³ rheumatic diseases,^72,74 periodontal diseases,⁷⁵ dacryocystitis,⁷⁶ thyroid disorders^70,77,78 and even neoplasms: thyroid13 and parathyroid tumors, melanomas^79,80 and breast tumors.⁸¹

Canadian researchers have recently confirmed that infrared imaging of breast cancer may detect small temperature changes associated with blood flow, showing abnormal patterns as the tumor grows. This occurs due to nitric oxide, a powerful vasodilator. Breast thermograms were positive in 83% of the cases against 61% on isolated clinical examination and 84% on mammography. The sensitivity of mammography (84%) increased to 95% when it was combined with infrared imaging. It is estimated that thermal imaging allows earlier diagnosis of breast cancer than mammography owing to the vasodilation produced by nitric oxide, which might occur 8 to 10 years before calcification is detectable through mammography.⁸¹

On account of such multiple applications, infrared thermometry can diagnose problems that affect different systems (neurological, vascular, muscular) in one single exam.^8,10 This method requires no contrast medium, since the warm blood itself, which circulates through cutaneous microcirculation, produces contrast for high-resolution images.

MINIMAL REQUIREMENTS

As in any diagnostic method, minimal requirements must be met.

Examination room

Standardized room conditions are essential for performing thermography.^5,66 The temperature must be kept at 22 oC and heat loss through forced-air convection directly over the patients should be averted. The speed of air incidence, if applicable, should not exceed 0.2 m/s.⁸² The patient must be kept away from electrical equipment that generate heat. The oscillation of room temperature should not be greater than 1 oC in a 20-minute period.

The air conditioner should have sufficient capacity to warm up the room. If possible, the exam should be carried out in a room with no windows; otherwise, the windows must be double-glazed and have external screens or shields to shut out sunlight. Fluorescent lamps (cold light) should be preferred to tungsten lamps. A digital thermometer, with a display that can be read from at least three meters away, should be available in order to monitor the place where the patient is. The thermometer should be placed in such a way that it is not directly influenced by heat sources.

Patient preparation

Preparation of patients is the most important parameter and demands careful attention.^5,66 It is of paramount importance that patients avoid taking hot baths or showers, using topic agents, creams, talcum powder, and doing vigorous exercises or physical therapy at least two hours before the exam. Patients should preferably have fasted for three hours and should not have taken stimulants, caffeine-rich substances or used nasal decongestants.

Once these requirements are met, patients are asked to undress the area to be examined. At least 15 minutes of exposure should be allowed so that the skin and room temperatures reach a balance. Patients may be asked to stand or sit down, depending on the area to be examined.

Infrared sensor specifications

In order that high-quality images can be obtained for clinical interpretation, the equipment must comply with the following minimal requirements:
" FPA (Focal Plane Array) detector;
" Spectral range of FPA detectors between 7.5 to 13 μm;
" detector with 320x240 pixels;
" instant spatial resolution of 0.6 mm to 50 cm;
" image quality that allows distinguishing anatomic details (e.g.: hair fiber);
" minimal operating range of 2 oC (span);
" average temperature adjustment between 5 and 45 oC (level);
" sensor with thermal sensitivity of 0.02 ºC;
" capacity to capture high-resolution gray-scale images;
" optics that allows capturing images showing both sides of the body;
" 14-bit radiometric video output;
" digital image online recording (14 bits) at least at 7 Hz;
" image storage for future reference and comparison;
" image processing software that operates within adjustable parameters, allows for thermal image subtraction and guarantees diagnostic quality;
" certificate of calibration issued by the National Institute of Standards and Technology (NIST, USA) or equivalent;
" Manufacturer's certificate of compliance in cases of OEM (Original Equipment Manufacturer);
" Infrared sensor update rate of 60 Hz (non-interlace).

During the exam, the equipment must be stabilized for 10 minutes before thermograms are obtained.

For accurate diagnosis, it is crucial that infrared thermometry be performed by a specially trained and qualified professional, and that all minimal requirements be met. Only good-quality information can be used as an ancillary tool for accurate diagnosis and follow-up of diseases.

One should not forget that the results obtained from infrared thermometry have to be properly correlated with the complete clinical history of the patient, a well-conducted physical examination and other diagnostic studies, when indicated. This way, thermal imaging may serve as a decisive tool in the establishment of a precise diagnosis and more accurate prognosis of patients with vascular disorders.

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