Reverse Engineering of Thermoregulatory Cold-Induced Vasoconstriction/Vasodilation During Localized Cooling
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applied sciences Article Reverse Engineering of Thermoregulatory Cold-Induced Vasoconstriction/Vasodilation during Localized Cooling Ali Youssef 1 , Anne Verachtert 1, Guido De Bruyne 2 and Jean-Marie Aerts 1,* 1 Department of Biosystems, Animal and Human Health Engineering Division, M3-BIORES: Measure, Model & Manage of Bioresponses Laboratory, KU Leuven, Kasteelpark Arenberg 30, 3001 Heverlee, Belgium 2 Department of Product Development, University of Antwerp, 2000 Antwerp, Belgium * Correspondence: [email protected] Received: 10 July 2019; Accepted: 8 August 2019; Published: 16 August 2019 Abstract: Biological systems, in general, represent a special type of control system. The physiological processes of homeostasis, which serve to maintain the organism’s internal equilibrium against external influences, are clear forms of biological control system. An example of the homeostasis is the control of the organism thermal state or the thermoregulation. The thermoregulatory control of human skin blood flow, via vasoconstriction and vasodilation, is vital to maintaining normal body temperatures during challenges to thermal homeostasis such as localised cooling. The main objective of this paper is to reverse engineer the localised thermoregulatory cold-induced vasoconstriction/vasodilation (CIVC/CIVD) reactions using a data-based mechanistic approach. Two types of localised cooling were applied to the fingers of 33 healthy participants, namely, continuous and intermittent cooling. Modelling of the thermoregulatory cold-induced vasoconstriction/vasodilation reactions suggested two underlying processes, with one process being 10 times faster. A new term is suggested in this paper, namely, the latent heat of CIVD, which represents the amount of dissipated heat required to trigger the CIVD. Moreover, a new model for the thermoregulatory localised CIVC/CIVD reactions is proposed. The suggested new model states that, with an initial vasodilation state, the initial localised CIVC is triggered based on a certain threshold in the rate of heat dissipation from the skin to the surrounding environment. Keywords: thermoregulation; homeostasis; cold-induced-vasodilation; cold-induced-vasoconstriction; control system; dynamic modelling 1. Introduction Biological systems represent a special type of control system. In all of these, control is exercised over the flows of matter and energy to maintain a range of stationarity of their existence [1]. Hence, all living organisms are equipped with numerous interconnected control systems, which serve to maintain the organism’s internal equilibrium regardless of outside influences. This condition is known as homeostasis. In the 19th century, Claude Bernard discovered the “amazing constancy” of the internal environment of the organism [2], and in 1927, Cannon named it the homeostasis [3]. An example of homeostasis is the control of an organism’s thermal state (thermoregulation system). Heat in biological systems is generated in the course of metabolic conversion and scattered by conduction, convection, radiation and evaporation [4–6]. The hands and feet form powerful thermoregulatory regulators in the body, serving as heat radiators (exchanger) and evaporators in hot environments and as thermal insulators in the cold [7]. Taylor et al. [8] estimated that each hand and foot can dissipate 150–220 W m 2 through radiation and · − Appl. Sci. 2019, 9, 3372; doi:10.3390/app9163372 www.mdpi.com/journal/applsci Appl. Sci. 2019, 9, 3372 2 of 19 Appl. Sci. 2019, 9, x FOR PEER REVIEW 2 of 19 convection at rest in an ambient temperature of 27 ◦C, with even greater heat dissipation through sweating.sweating. Additionally,Additionally, the the extremities extremities can servecan asserv thermale as thermal sensor acting sensor in feedbackacting in and feedback feedforward and fashionfeedforward to the fashion thermoregulation to the thermoregulation system of the system body [7 of]. the body [7]. ArteriovenousArteriovenous anastomosesanastomoses (AVAs) (AVAs) are are direct direct connections connections between between small small arteries arteries and small and veinssmall (Figureveins (Figure1), with 1), no with capillary no capillary section betweensection between them. Since them. there Since is nothere capillary is no capillary transportation, transportation, the only transportthe only transport function they function could they possibly could have possibly is the have transport is the of transport heat from of the heat body from core the to surfacebody core areas to containingsurface areas AVAs containing [9]. AVAs [9]. Figure 1. Schematic diagram showing the effect of a closed (A) and an open (B) arteriovenousFigure 1. Schematic anastomoses diagram on theshowing blood flowthe effect during of cold-induced a closed (A vasoconstriction) and an open ( andB) arteriovenous cold-induced vasodilation,anastomoses respectively.on the blood flow during cold-induced vasoconstriction and cold-induced vasodilation, respectively. Grant and Blond [10] investigated the role of AVA in thermoregulation. They found a relation betweenGrant the and number Blond of [10] AVAs investigated in a body the part role and of theAV changeA in thermoregulation. in local skin temperature They found due a torelation local coldbetween [11]. the When number the of extremities AVAs in ofa body the handpart and and th feete change are exposed in local locally skin temperature to a cold environment, due to local theircold [11]. AVAs When respond the withextremities sympathetically of the hand mediated and feet vasoconstriction,are exposed locally which to a iscold termed environment, cold-induced their vasoconstrictionAVAs respond (CIVC).with sympathetically CIVC reduces themediated blood flow vasoconstriction, to the peripheries which in favour is termed of a central cold-induced pooling ofvasoconstriction blood in the torso (CIVC). and CIVC deep bodyreduces core the [7 blood,12,13]. flow Due to to the this peripheries vasoconstriction in favour and of a the central high pooling surface area-to-volumeof blood in the torso ratio, and the skindeep temperature body core [7,12,13]. of the extremities Due to this tends vasoconstric and exponentiallytion and the decreases high surface to a levelarea-to-volume approaching ratio, that the of the skin ambient temperature environment. of the extremities After a brief tends period and of exponentially lowered skin blood decreases flow andto a temperature,level approaching due to that the CIVC,of the aambient temporary environment. increase in After blood a flow brief and period rewarming of lowered occurs. skin During blood these flow and temperature, due to the CIVC, a temporary increase in blood flow and rewarming occurs. During episodes, skin temperature can rise by as much as 10 ◦C, and this fall and rise can occur repeatedly in a cyclicthese fashionepisodes, [7 ].skin This temperature pattern of periodiccan rise warmingby as much was as first 10 reported°C, and bythis Lewis fall and [14], rise who can labelled occur itrepeatedly the “hunting in a response”,cyclic fashion due [7]. to This its apparent pattern of oscillatory periodic warming pattern. Thiswas responsefirst reported is also by termedLewis [14], the cold-inducedwho labelled it vasodilation the “hunting (CIVD) response”, phenomenon due to its [15 apparent]. There oscillatory is a definite pattern. variation This in response the occurrence, is also magnitude,termed the andcold-induced duration ofvasodilation the CIVD[ 16(CIVD)]. phenomenon [15]. There is a definite variation in the occurrence,It was found magnitude, that the and CIVD duration occurs inof aboutthe CIVD 5 to 10[16]. min after the exposure of the hand to cold [15,17], and isIt initiatedwas found by thethat dilation the CIVD of theoccurs AVAs in [about7,13,15 5, 18to]. 10 Because min after ofthe the elevated exposure extremity of the hand blood to flowcold and[15,17], temperature, and is initiated CIVD hasby the generally dilation been of presumedthe AVAs to[7,13,15,18] provide a. protectiveBecause of function the elevated by maintaining extremity localblood tissue flow integrityand temperature, and minimizing CIVD has the generally risk of cold been injuries. presumed However, to provide the mechanisms a protective underlyingfunction by CIVDmaintaining are unclear, local tissue yet understanding integrity and minimizing the nature ofthe CIVD risk of is cold of important injuries. However, occupational the mechanisms and clinical relevanceunderlying [7 ].CIVD Additionally, are unclear, the yet review understanding studies of Cheung the nature et al. of [7CIVD,19] have is of shown important that itoccupational is not easy toand compare clinical direlevancefferent research [7]. Additionally, findings duethe review to the inconsistentstudies of Cheung methodologies et al. [7,19] in have the experimentalshown that it protocols,is not easy and to mostcompare of the different studies onresearch CIVD arefindings largely due descriptive, to the inconsistent lacking suffi cientmethodologies quantification in the of CIVDexperimental responses. protocols, and most of the studies on CIVD are largely descriptive, lacking sufficient quantification of CIVD responses. The current study was originated based on the findings of previous study by Youssef et. al. [20], in which the authors tried to take advantage of the CIVC reaction to prevent nail toxicity during Appl. Sci. 2019, 9, 3372 3 of 19 Appl. Sci.The 2019 current, 9, x FOR study PEER was REVIEW originated based on the findings of previous study