Using Thermography in the Diagnostics of Lymphedema: Pilot Study

Abstract

Purpose:

The aim of the study was to evaluate the usefulness of thermography in the diagnosis of lymphedema.

Methods:

The study included 43 women after axillary dissection caused by breast cancer, whose mean age was 64.4 ± 7.8 years. The subjects were divided into two groups, with the criterion for division being the appearance of secondary lymphedema. The size of lymphedema was verified by Limb Volumes Professional 5.0; body surface temperatures were registered using a thermal camera.

Results:

In the control group, the difference in the volume of the limb on the operated side and the contralateral limb was 7.5 ± 77.7 mL (3.6%). The temperature on the nonoperated side tended to be higher than on the opposite side. In the test group, the difference in size between the limbs was 54.5 ± 312.7 mL (29.3%). In the case of mild or moderate edema, a reverse tendency was observed. While measuring the difference in the mean surface temperatures of both limbs belonging to two groups, a significance of differences at the level of p = 0.04 was observed. Moreover, a negative Spearman correlation coefficient (−0.34) was observed between the size of secondary lymphedema and the surface temperature.

Conclusion:

Noninvasive thermography can provide a valuable supplementary tool in the diagnostics of secondary lymphedema.

Introduction

Lymphedema is a chronic debilitating disease that never remits spontaneously. It is often misdiagnosed, diagnosed too late, or completely untreated.¹ Apart from constituting a health risk, it also negatively impacts on the socioeconomic situation.^2,3 The disease affects more than 90 million people worldwide, especially in Asia and the Far East. In developed countries, the primary cause of lymphedema is radiation therapy, most often used during the treatment of breast cancer, gynecologic cancers, prostate cancer, cancers of the urinary system, head and neck, as well as melanoma, sarcoma, and lymphoma.^1,3

Secondary lymphedema develops as a result of abnormal accumulation of lymph fluid in the tissue; as it progresses, the extensibility of the subcutaneous tissue decreases. Apart from changes in the volume or circumference of the affected area, patients suffer from a feeling of heaviness, reduced mobility, trophic changes in the skin, and recurrent cellulitis. Consequently, it leads to the development of tissue fibrosis.⁴

One of the main factors affecting the effectiveness of lymphedema treatment is the fast and correct diagnosis; however, there are no commonly accepted standards in this regard.⁵ The most common methods of diagnostics include circumference measurements, water displacement, tissue tonometry, perometry, bioimpedance spectroscopy, contrast-enhanced magnetic resonance lymphangiography, and indocyanine green lymphangiography.⁶

Thermography is a medical imaging method that has been used increasingly often in recent years. It is a completely safe, noninvasive, and noncontact method that makes it possible to determine the distribution of body surface temperatures, which are often connected with the physiological or pathological condition of tissues or organs.^7,8

Thermal phenomena on the surface of the human body result from metabolic changes in the subcutaneous tissue, the blood supply to the tissue, thermal conductivity of the muscular and adipose tissues, and the exchange of heat with the environment through skin.^9,10 Morbidities, especially inflammations, change the heat flow rate, which results in a large temperature gradient between the affected area and the symmetrical body area.⁷ Thus, noncontact thermography can provide excellent support for the traditional screening methods. Moreover, due to the possibility of analyzing the distribution of body surface temperatures, thermography can be considered a supplementary method in the diagnostics of lymphedema.⁸

This study was intended to assess the usefulness of thermography in the diagnostics of lymphedema. It was assumed that the temperature of surface tissues is connected with the stage of lymphedema, and consequently that noncontact thermography can be used as a method complementing other diagnostic methods.

Test Group

The study included 43 women after axillary dissection caused by breast cancer, whose mean age was 64.4 ± 7.8 years. The average height was 159.8 ± 5.6 cm, and average body weight was 74.8 ± 10.9 kg. A total of 83.7% of the subjects had undergone mastectomy, while 16.3% had had breast-conserving surgery. Moreover, 51.2% of the research participants had been subjected to radiotherapy, 55.8% had undergone chemotherapy, and 48.8%—hormonal therapy. The average time since the treatment was 7.9 ± 6.3 years. The subjects were divided into two groups, with the criterion for division being the appearance of secondary lymphedema (detailed analysis of the studied groups is presented in Tables 1 and 2).

Table 1.

Descriptive Characteristics of the Studied Groups

Variable	Test group, N = 20	Control group, N = 23	p
Age, years	64.4 ± 8.6	64.4 ± 7.2	0.79
Body weight, kg	74.6 ± 12.3	74.8 ± 9.8	0.80
Height, cm	159.2 ± 4.5	160.2 ± 6.4	0.63
Time since treatment, years	9.4 ± 6.8	9.2 ± 5.8	0.78

Table 2.

Treatment Used in the Studied Groups

Variable	Test group (N = 20), %	Control group (N = 23), %	χ² Pearson—p
Mastectomy	75.0	91.3	0.14
Radiotherapy	70.0	34.8	0.02
Chemotherapy	70.0	43.5	0.08
Hormonal therapy	50.0	47.8	0.88

The test group was also verified for the size of lymphedema. In eight women it was mild (the size of the edema was 10%–20%), in eight—moderate (the size of the edema was 20%–40%), and in four women—severe, with the size of the edema greater than 40%.

The research was approved by the Senate Committee on Ethics of Scientific Research at the University School of Physical Education (June 28, 2007).

Informed consent was obtained from all individual participants included in the study.

The authors of the research obtained consent from the persons examined with the probe to participate in the research.

Research Methods

Assessment of the size of lymphedema

In all the women, the circumference of both upper limbs was measured at five points with the use of a measuring tape. The first measurement was made at the height of the ulnar styloid process, and the four subsequent measurements were made at 10-cm intervals, beginning from the styloid process. The examination was performed in the standing position, with the upper limb held at a 90° angle and resting on wall bars. The size of lymphedema, expressed in milliliters and as a percentage, was obtained with the use of Limb Volumes Professional 5.0 software. To assess the severity of secondary lymphedema, the following criteria were applied:

no edema—below 10%

mild edema—10%–20%

moderate edema—20%–40%

severe edema—above 40%

Registration of body surface temperatures

Body surface temperatures were registered with the use of thermal camera ThermoVision FLIR SYSTEMS T335 connected to a personal computer with the Therma CAM Researcher 2.9 software installed. All the measurements were made in identical conditions. The measurements of the minimal, maximal, and average temperatures of a given body area were taken in the standing position, from the front and from the back side of the body, at a distance of 2 m. Before making the thermograms, the patients remained without outerwear for ∼10 minutes to balance the body temperature. A quantitative and qualitative analysis of the thermograms was performed for 16 body regions (Fig. 1), for areas of the upper limbs on the postoperative side and the contralateral side (from the front and back).

FIG. 1.

Description of measurement areas.

For the needs of the statistical analyses, the results of the front and back thermograms were averaged for the limb on the operated side and the contralateral limb, so that two results were eventually compared.

Statistical analysis

The statistical analysis was performed using Statistica 10.0 software. Normality of distribution was verified with the Shapiro–Wilk test, while Levene's test was used to assess the equality of variances. The Mann–Whitney U test was used to determine whether two independent samples were selected. The analysis for comparing multiple independent samples was conducted on the basis of the Kruskal–Wallis test and Dunnett's test. Moreover, the chi-squared test was used, and Spearman's rank correlation was calculated. Results at a level p < 0.05 were considered to be statistically significant.

Results

In the control group, the difference in the volume of the limb on the operated side and the contralateral limb was 7.5 ± 77.7 mL (3.6%), while in the test group, irrespective of the size of edema, it was 54.5 ± 312.7 mL (29.3%) (p < 0.01, Mann–Whitney U test). The results for each size of the edema are presented in Table 3.

Table 3.

The Significance of Differences in the Size of the Edema in Both the Studied Groups (Kruskal–Wallis Test)

	Control group (1)	Mild edema (2)	Moderate edema (3)	Severe edema (4)
Edema size	70.5 ± 77.7 mL	322.3 ± 126.6 mL	614.8 ± 136.7 mL	1098 ± 37.4 mL
Edema size	3.6%	16.3%	29.8%	54.3%
1		p = 0.02	p < 0.01	p < 0.01
2	p = 0.02		p = 1.00	p = 0.35
3	p < 0.01	p = 1.00		p = 1.00
4	p < 0.01	p = 0.35	p = 1.00

Figure 2 shows the analysis of temperature distribution for both upper limbs (the limb on the operated side vs. the contralateral limb) in each group. In the control group, it was observed that the temperature on the nonoperated side tended to be higher than on the opposite side. In the test group, particularly in the case of mild or moderate edema, a reverse tendency was observed—the surface temperatures were higher on the operated side, which was more edematous. However, the differences were not statistically significant (Mann–Whitney U test).

FIG. 2.

Distribution of average body surface temperatures within both limbs for individual group.

While measuring the difference in the mean surface temperatures of both limbs in subjects belonging to the control group and the test group, a significance of differences at the level of p = 0.04 was observed (Mann–Whitney U test, Fig. 3).

FIG. 3.

The distribution of the difference in average surface temperatures for both groups.

Regarding the size of secondary lymphedema, it was observed that the average surface temperatures of the tested upper limbs tended to increase in parallel to the size of lymphedema, until the moderate size. In case of severe secondary lymphedema, the difference in surface temperatures decreased. The distribution of average body surface temperatures in the tested limbs is shown in Figure 4, while detailed data are presented in Table 4.

FIG. 4.

The distribution of average body surface temperatures in upper limbs in the studied groups depending on the size of secondary lymphedema.

Table 4.

The Significance of Differences Between the Studied Groups Depending on the Size of Secondary Lymphedema with Regard to the Average Difference in Body Surface Temperatures of Upper Limbs (Dunnett's Test)

	Control group (1)	Mild edema (2)	Moderate edema (3)	Severe edema (4)
Difference in temperatures, °	−0.09 ± 0.4	0.11 ± 0.2	0.2 ± 0.3	0.05 ± 0.4
p		0.23	0.07	0.48

Moreover, a negative Spearman correlation coefficient (−0.34) was observed between the size of secondary lymphedema and the surface temperature.

Discussion

Secondary lymphedema is a serious complication observed in patients treated for cancers; it is estimated to develop in ∼50% of patients undergoing lymphadenectomy.¹¹ Secondary lymphedema is considered to be a disease caused by damage to the lymphatic system, which is characterized by a complex pathophysiological chain. At the early stages, the deposition of interstitial fluid is obstructed as a result of lymphostasis, which gradually leads to a chronic inflammatory state of lymphatic vessels and their impairment; it results in adipose tissue deposition and fibrosis.^12,13 All of this leads to the classification of lymphedema as a chronic and irreversible condition. The inflammation is an essential component for the development of lymphedema, especially T cell-mediated pathogenesis. Inflammatory cytokines have been implicated in both the development of fibrosis and adipose tissue deposition.¹³

In the research, it was observed that surface temperatures in the edematous limb tended to be higher, particularly visible in moderate edema. Moreover, the average difference in surface temperatures between the control group and the test group was significant. The results are compatible with the previous research by Clodius et al.¹⁴ Lymphedematous limb was found to have an increased temperature up to 2°C. In addition, the skin of the lymphedematous arm in ∼70% of the patients was found to be drier than the normal one.¹⁴ Lymph stasis leads to chronic inflammation with destruction of elastic fibers, stimulation of fibroblasts, keratinocytes, and adipocytes, increased production of collagen, and accumulation of glycosaminoglycans causing hypertrophy of the skin and subcutaneous tissue.¹⁵ Ammer also reported higher skin temperature on the edematous side (of about 0.02°C) compared with the opposite healthy side, but in this case only for primary edema.¹⁶ However, for secondary lymphedema, in women treated for breast cancer, lower skin temperature in the swollen arm was reported, on average 1.3°C cooler than the healthy side. Mean difference in circumference between the examined limbs was only 0.7 cm.¹⁶ According to the accepted standards, such a difference does not indicate lymphedema but only the latent stage of lymphedema development without clinical symptoms.¹⁶ Stanton et al. documented decreased skin blood flow in lymphedematous arm, which may suggest a rather lower skin temperature. However, this may be affected by lymphadenectomy that directly results in lymph circulation disorder in the flow area and in the initial stage of the edema development (latent edema). This may affect the surface skin temperature.¹⁷ This aspect might have influenced the differences between the conducted researches.

The literature on the purposefulness of using thermographic methods emphasizes the possibility of fast analysis of pathological processes in tissues by means of an increase in temperature visible in thermograms. Registering hyperthermia in thermal examined areas can be caused by an inflammatory state.¹⁸ An inflammatory state is observed in the initial stage of lymphedema and is defined as an essential component for the development of lymphedema.¹³

To estimate the dynamism of temperature changes in inflammatory states, the usefulness of the thermographic method in the diagnostics and assessment of infrared emission of the soft tissues has been demonstrated even in the initial stages of the inflammatory process.^19,20

A significant increase in temperature in comparison with the contralateral area (without inflammatory state) is observed in professional sportspeople after injuries to the active motor organ of various etiologies.^21–23 Significant changes in skin surface temperatures have been shown in tests of inflammatory states in dental surgery.^24,25

The data above indicate the usefulness of thermography in the diagnostics of lymphedema. Thermographic screening tests seem to be justifiable in the monitoring of changes in patients exposed to a greater risk of developing lymphedema due to prior cancer treatment, particularly in the latent stage of lymphedema development, when there are no clinical symptoms despite the ongoing changes in lymphatic vessels.

It is noteworthy that in the presented research, further analysis indicated a decrease in body surface temperatures in the severe stage of secondary lymphedema. Asymmetrical distribution of body surface temperatures could be analyzed from the point of view of hyperthermia. Reduced blood flow, decreased muscle activeness, degeneration of soft tissues due to prolonged damage, chronic tendon injury, and keloidal scars manifest themselves in decreased surface temperatures (hyperthermia) of the analyzed area.^26,27 Apart from significant limb edema, advanced stages of lymphedema lead to the fibrosis of skin and subcutaneous tissue. Skin fibrosis is a clinically serious pathological process of secondary lymphedema.²⁸ Moreover, muscular dystrophy is caused by the disposition of adipose tissue. The dysfunctional adipose tissue and its secretion products can worsen lymphatic vessels' function, aggravating lymph leakage and stagnation, which can promote further adipose tissue deposition and fibrosis, similar to what may happen in obesity.^21,29 It is assumed that body composition (in particular the adipose content) and skin thickness of the tested areas can serve the role of heat insulators, and thus make heat dissipation more difficult. Due to decreased heat conductivity and simultaneously greater volume of the insulator, the size of skin and fat folds and the thickness of adipose tissue in the body provide insulation barrier to heat conductivity. It can decrease the body's ability to effectively react to changes in the environmental temperature. A correlation between temperature decrease and the subjects' body fat percentage was demonstrated by Dębiec-Bąk et al.³⁰ and Chudecka et al.³¹

Analyses of the physiological mechanisms of body temperature control conducted in recent years have generated a broad diagnostic spectrum, both in treatment and physiotherapy. The advancement of thermography makes it possible today to precisely detect and locate thermal disorders characterized by increased or decreased body surface temperatures. Injuries, disease processes, and their secondary consequences cause changes in blood flow, and indirectly affect the body surface temperature.^24,32 This method should also be considered in the diagnostics of lymphedema.

Limitations

The above information appears to confirm the purposefulness of using thermography not only in the early stages of lymphedema development but also in the diagnostics of lymphedema severity. To confirm the above procedures, prospective research on a bigger research sample should be conducted.

In addition, it is important to determine the specific etiology of edema. Infection is a frequent sequel of edema and causes increased capillary permeability. This aspect was not included in the research, as in the history of lymphedema development, skin infection was not recorded. The patients did not report any complications or skin inflammation in the edematous limb during the examination.

Conclusions

Noninvasive thermography may support a clinical diagnosis of lymphedema both within screening test models and tests connected with structural changes connected with the evaluation of the stage of lymphedema.

Compliance with Ethical Standards

Ethical approval

All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

The study received ethical approval from the Senate Committee on Ethics of Scientific Research at the University School of Physical Education (June 28, 2007).

Informed consent

Informed consent was obtained from all individual participants included in the study.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

Funding Information

The research project was made from covered funds and no funding was received from other institutions.

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