Abnormal thermography in Parkinson's disease

https://doi.org/10.1016/j.parkreldis.2015.05.006Get rights and content

Highlights

  • In Parkinson's disease (PD) there is an involvement of the peripheral autonomic nervous system.

  • We investigated cutaneous thermoregulation in PD using skin thermography and cold stress test.

  • PD patients reveal abnormal skin thermal responses in thermography, suggesting cutaneous autonomic dysfunction.

  • Skin thermography may have major potential in the evaluation of skin sympathetic dysfunction in PD.

Abstract

Background

An autonomic denervation and abnormal vasomotor reflex in the skin have been described in Parkinson's disease (PD) and might be evaluable using thermography with cold stress test.

Methods

A cross-sectional pilot study was undertaken in 35 adults: 15 patients with PD and abnormal [123I]-metaiodobenzylguanidine cardiac scintigraphy and 20 healthy controls. Baseline thermography of both hands was obtained before immersing one in cold water (3 ± 1 °C) for 2 min. Continuous thermography was performed in: non-immersed hand (right or with lesser motor involvement) during immersion of the contralateral hand and for 6 min afterward; and contralateral immersed hand for 6 min post-immersion. The region of interest was the dorsal skin of the third finger, distal phalanx.

Results

PD patients showed a lower mean baseline hand temperature (p = 0.037) and greater thermal difference between dorsum of wrist and third finger (p = 0.036) and between hands (p = 0.0001) versus controls, regardless of the motor laterality. Both tests evidenced an adequate capacity to differentiate between groups: in the non-immersed hand, the PD patients did not show the normal cooling pattern or final thermal overshoot observed in controls (F = 5.29; p = 0.001), and there was an AUC of 0.897 (95%CI 0.796–0.998) for this cooling; in the immersed hand, thermal recovery at 6 min post-immersion was lesser in patients (29 ± 17% vs. 55 ± 28%, p = 0.002), with an AUC of 0.810 (95%CI 0.662–0.958).

Conclusions

PD patients reveal abnormal skin thermal responses in thermography with cold stress test, suggesting cutaneous autonomic dysfunction. This simple technique may be useful to evaluate autonomic dysfunction in PD.

Introduction

The diagnosis of Parkinson's disease (PD) is based on motor symptomatology; however, it is accompanied or preceded by non-motor manifestations, including autonomic dysfunction [1].

In Lewy bodies diseases there is an early involvement of the peripheral autonomic nervous system, as demonstrated in pathology studies [2], [3] and in autonomic studies using cardiac functional imaging [3], [4] or other cardiovascular function tests [1], [3], [5]. Cardiac scintigraphy with [123I]-metaiodobenzylguanidine (MIBG) is the autonomic test most frequently used for PD diagnosis in the clinical setting [6]. Biopsies have recently been validated for this purpose in various organs, including the skin [7], [8].

Skin biopsies have revealed autonomic denervation (blood vessels, sweat glands, Meissner's corpuscles, piloerector muscle, etc.), which is predominantly noradrenergic with alpha-synuclein deposits [7], [8], [9]. Body temperature control largely depends on the skin, with or without central control, via sudomotor and subcutaneous arteriolar and vasomotor sympathetic functions [10]. Thermoregulation is altered by central and/or peripheral autonomic involvement in PD [11], [12]. Many PD patients have sweat disorders and temperature intolerance. They occasionally experience cold limbs phenomena, which have been related to prolonged vasoconstriction due to post-denervation noradrenergic hypersensitivity [13]. This alteration of the skin vasomotor reflex (SVR), measured with a doppler flowmeter, is common in Lewy bodies diseases after different adrenergic stimuli [12].

High-definition infrared thermography is currently used to study diseases with skin vasomotor dysfunction, including Raynaud's syndrome [14], [15] and diabetic polyneuropathy [16], [17]. Various authors have combined thermography with a stimulus such as cold (Cold Stress Test [CST]) to quantify thermal reduction in relation to sympathetic vasoconstriction and subsequent thermal recovery [14], [16], [18], which are typically altered in autonomic neuropathies [16]. Thermographically measured skin temperature is an indirect measurement of the blood flow, as verified by doppler flowmetry after the immersion of one hand in cold water [18].

We hypothesized that involvement of the peripheral autonomic nervous system in PD may manifest as an altered cutaneous thermoregulation. We investigated whether hand thermography with CST may have potential for the evaluation of skin autonomic dysfunction in PD.

Section snippets

Subjects

A cross-sectional pilot study was undertaken in 35 adults: 15 patients with PD fulfilling diagnostic criteria according to UK Brain Bank and with postganglionic sympathetic cardiac denervation supported by a recent (<6 months earlier) scintigraphy with [123I]-MIBG [19], selected by convenience sampling from among participants in a previous study on autonomic nervous system evaluation in our unit; and 20 healthy relatives of patients in our hospital as controls. All patients had sporadic,

Baseline characteristics

Table 1 shows the characteristics of the PD patients with cardiac denervation in [123I]-MIBG scintigraphy (normal delayed H/M ratio value at our center is 2.03 ± 0.32; cutoff value is 1.51) [19]. Table 2 lists the thermographic characteristics and variables at baseline. All participants were right-handed. PD patients were older than controls (71.8 ± 5.94 vs. 67.1 ± 7.13 yrs; p = 0.036) and more frequently showed subjective hyposmia (67% vs. 14%; p = 0.002). There were no differences between the

Discussion

The main finding of this study was that hand thermography differed between PD patients with sympathetic cardiac denervation and controls at baseline and in response to cold.

During the contralateral hand CST (test A), the NIH of the patients did not show the normal cooling and thermal overshoot observed in the controls. Furthermore, after immersion (test B), the thermal reduction and recovery were lower in the IH of patients than in that of controls. In both tests, the lesser cooling in the NIH

List of authors and their contributions to the manuscript

Antonio-Rubio: Design of study, acquisition of data, drafting and revision of the article, and final approval of the version to be submitted.

Madrid-Navarro: Design of study, acquisition of data, drafting and revision of the article, and final approval of the version to be submitted.

Salazar-López: Design of study, acquisition of data, revision of the article, and final approval of the version to be submitted.

Pérez-Navarro: Acquisition of data, revision of the article, and final approval of the

Disclosures

All authors report no disclosures.

Funding

The study was supported by grants from “Instituto de Salud Carlos III” of the Spanish Government (“Fondo de Investigación Sanitaria”, file 10/01819) and European Regional Development Fund (ERDF).

Acknowledgments

The authors are grateful to Luisa Fernanda Rodríguez Ferreira for her logistic support throughout the study.

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    These authors contributed equally to this study.

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