Cognitive decrements do not follow neuromuscular

Int. J. Hyperthermia, 2010, 1–10, Early Online

RESEARCH ARTICLE

Cognitive decrements do not follow neuromuscular alterations during passive heat exposure

Int J Hyperthermia Downloaded from informahealthcare.com by University of Queensland on 11/21/10 For personal use only.

NADIA GAOUA1, JUSTIN GRANTHAM1, FARID EL MASSIOUI2,3, OLIVIER GIRARD1, & SEBASTIEN RACINAIS1 1

Research and Education Centre, ASPETAR, Qatar Orthopaedic and Sports Medicine Hospital, Doha, Qatar, Laboratoire de Psychologie et de Neurosciences, Groupe IME, Paris, France and 3 Laboratoire Cognition Humaine et Artificielle, UFR de Psychologie, Universite´, Paris 8, France 2

(Received 26 April 2010; Revised 28 July 2010; Accepted 25 August 2010)

Abstract To investigate what triggers cognitive and neuromuscular alterations during passive heat exposure, eight volunteers performed simple (One Touch Stockings of Cambridge, OTS-4) and complex (OTS-6) cognitive tasks as well as neuromuscular testing (maximal isometric voluntary contractions of the thumb with electrical stimulation of the motor nerve and magnetic stimulation of the motor cortex). These tests were performed at the start (T1), after 1 h 30 min (T2), 3 h (T3) and 4 h 30 min (T4) of exposure in both hot (HOT) (Wet Bulb Globe Temperature [WBGT] ¼ 38" # 1.4" C) and neutral control (CON) (WBGT ¼ 19" # 0.3" C) environments. Environmental temperatures were adjusted during the HOT session to induce target core temperatures (Tcore) (T1 $ 37.3" ; T2 $ 37.8" ; T3 $ 38.3" ; T4 $ 38.8" C). At T1 and T4 the OTS-6 was lower in HOT than in CON in response to the rapid increase in skin temperature and to hyperthermia, respectively. In HOT, the increase in Tcore limited force production capacity possibly via alterations occurring upstream the motor cortex (from Tcore $ 37.8" C) but also via a decrement in motor cortical excitability (from Tcore $ 38.3" C). These alterations in cortex excitability failed to explain the cognitive alterations that can originate from an additional cognitive load imposed by temperature variations. Keywords: cognitive load, task complexity, temperature, thermoregulation, transcranial magnetic stimulation

Introduction The physiological responses to heat exposure and its consequences on health have been well documented. However, despite the number of studies conducted the impact of heat exposure on cognitive function remains equivocal. Methodological discrepancies between studies have made it difficult to conclude whether heat exposure does [1–5] or does not [6–8] adversely affect cognitive function and under what specific environmental and physiological conditions these alterations appear. Dehydration [9, 10] and exercise [11–13] can alter neuromuscular and cognitive functions. Therefore, passive heat exposure in a euhydrated state represents a useful model to investigate the effects of

hyperthermia upon cognitive and neurophysiological functions because it avoids any potential exerciserelated side effects. Passive heat exposure can decrease maximal voluntary contraction (MVC) force production due to a decrement in neural drive to the muscle [14–16]. This decrement in voluntary activation appears to be due to an elevated core temperature (Tcore) rather than from inputs from skin thermo-sensitive afferences. This assumption was partly confirmed when cooling the skin of hyperthermic volunteers did not have any beneficial effects on neuromuscular function [14–16]. In contrast, cognitive function is influenced by variations in skin temperature (Tskin) [17, 18]. While head cooling can preserve complex cognitive tasks during whole body hyperthermia [16], less than 30 min heat

Correspondence: Nadia Gaoua, Research and Education Centre, ASPETAR, Qatar Orthopaedic and Sports Medicine Hospital, Doha, Qatar. Tel: (þ974) 413 2578. Fax: (þ974) 413 2034. E-mail: [email protected] ISSN 0265–6736 print/ISSN 1464–5157 online ! 2010 Informa UK Ltd. DOI: 10.3109/02656736.2010.519371


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exposure has also been shown to induce decrements in cognitive performance that are unlikely to have originated from increases in Tcore [19]. Therefore, cognitive and neuromuscular alterations in hot environments do not appear to respond to the same triggers; however, the sequence in which these alterations occur is still unknown. Literature reviews typically suggest that complex tasks are more vulnerable to the effects of heat exposure than simple tasks [16–21]. However, different cognitive tasks assess numerous areas of the brain and comparing task complexity, ignores the varying cognitive loads placed on the different brain regions. Furthermore, each brain structural area has its own homeostatic temperature, with a dorsoventral temperature gradient being exhibited in most mammalian species including humans [22]. The hippocampus of rats at rest has a significantly ($0.7" C) lower temperature than the medial preoptic area of the hypothalamus [23]. Temperatures of both of these brain areas are directly correlated to Tcore and increase in a linear fashion [23], therefore, with an uncompensated thermal stress this suggests that at the same Tcore the absolute thermal load could be vastly different between brain areas. Therefore, the current experiment was designed to verify the hypothesis that decrements in neuromuscular and cognitive function will follow different patterns during prolonged passive hot exposure. Two complexity levels within the same task were investigated. This was done such that the mechanism required for successful task performance and the brain area being assessed would remain constant, but the cognitive load required to successfully complete the task would be manipulated.

Methods Subjects Eight volunteers (7 male and 1 female, 34 # 6 years, 76 # 11 kg and 175 # 5 cm for age, weight and height, respectively) participated in the study. All subjects were free from wrist or thumb injuries at the time of the experiment. Subjects were asked to avoid all vigorous physical activity for the 24 h preceding the test. This study was approved by the Institutional Ethics Committee and was designed in accordance with the 1964 Helsinki Declaration. General procedure To investigate the triggers and sequence of cognitive and neuromuscular alterations during passive heat exposure, eight volunteers remained in a hot environment (WBGT ¼ 38" # 1.4" C) for 5 h. Cognitive

and neuromuscular functions were tested four times (every 90 min) and compared to a control condition. One week before commencing the experimental sessions, subjects completed a familiarisation session. Using a counter-balance design, subjects then completed two 5-h experimental sessions each separated by at least four days of recovery. Both sessions were conducted at the same time of the day in an environmental chamber (Tescor, Warminster, PA), with constant noise, light (212 lx), and wind speed (0.5–0.6 m s&1) conditions. In both sessions subjects wore shorts and t-shirt and performed four test trials (including both cognitive and neuromuscular assessments). Water was provided ad libitum throughout both experimental sessions to maintain body weight within 1% of the pre-test value. Familiarisation session. Subjects were familiarised with the cognitive and neuromuscular testing protocols. The cognitive testing battery software (see below) provided a familiarisation procedure for the test, following which subjects performed the complete procedure. Each subject then performed several MVC of the abductor pollicis until they felt accustomed to the equipment; such that the coefficient of variation in three successive MVC trials was less than 5%. This session was also used to accustom the subjects to the electrical stimulation of the motor nerve and to the transcranial magnetic stimulations (TMS) procedures. Control session (CON). After 20 min of rest (for electrode placement, verification of the signals and stabilisation of the values), subjects entered the environmental chamber where they performed a trial every 90 min (T1 upon entry in the room; T2 after 1 h 30 min; T3 after 3 h; T4 after 4 h 30 min). During each trial, subjects performed a planning task (OTS) and MVC of the right abductor pollicis with superimposed electrical stimulation of the motor nerve and TMS. The room was set at 24" C and 40% relative humidity (rH) and the average WBGT recorded (QUESTempo36, Quest Technologies, Oconomowoc, WI) during the session was 19.1" # 0.3" C. Hot session (HOT). The procedure was the same as CON, but with the room initially set at 44" C and 40% rH. The room temperature was then adjusted (temperatures ranging between 44" and 48" C) so that each subject obtained a target Tcore for each trial (T1 $ 37.3" ; T2 $ 37.8" ; T3 $ 38.3" ; T4 $ 38.8" C). The average WBGT recorded during HOT was 38.3" # 1.4" C.

Cognitive and neuromuscular alterations


Temperature recording Tcore and Tskin (hand and chest) were monitored " using the VitalSense system (precision 0.01" C, Mini Mitter, Respironics, Herrsching, Germany). TM A wireless Mini Mitter Jonah ingestible thermometer pill was swallowed at least 5 h before each trial to measure Tcore. The validity of ingestible thermometers to monitor Tcore has been confirmed during both rest and exercise, making them a viable substitute to more invasive methods [24]. Chest (Tchest) and hand (Thand) skin temperatures were monitored with XTP wireless adhesive dermal temperature patches. Both Tcore and Tskin sensors sent data by telemetry to the same data logger every 60 s. In both conditions a timestamp for each temperature variable was recorded before and after the commencement of the cognitive trials at T1, T2, T3 and T4. Cognitive testing A planning task (OTS) was performed in a seated position during each trial using Cantab software (CANTABeclipse, Cambridge Cognition, Cambridge, UK) and hardware (33.8 cm tactile screen and touch pad) in the environmental chamber. Subjects were shown two displays containing three coloured balls. The displays were presented in such a way that they could be perceived as stacks of coloured balls held in stockings suspended from a beam. Along the bottom of the screen there was a row of numbered boxes. Subjects were initially shown how to move the balls in the lower display to copy the pattern in the upper display. The experimenter completed one demonstration problem, where the solution required one move, following which the subjects completed three further practice problems, one each of two, three and four moves before starting the test. For the test itself, subjects were shown further problems, and had to mentally calculate the minimum number of moves required to solve the problems, and then to touch the corresponding box at the bottom of the screen to indicate their response. The outcome measures were the number of problems solved on the first choice for two different levels of complexity that required four (OTS-4, simple) and six moves (OTS-6, complex). Each measure was obtained by averaging the score obtained over four trials. Neuromuscular testing The maximal thumb force was recorded using a custom-designed ergometer. Subjects were seated in an upright position with their hand on an ergonomic support. Subjects were requested to abduct their right thumb and maximally press on a strain gauge. The force recorded primarily involved the abductor

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pollicis longus as well as assistance from the flexor digitorum manus perforans and the musculus opponens pollicis. For each recording, the average of six MVC of 3 s was recorded. During three of the six MVC, the motor nerve was further activated by superimposed electrical stimulation of the posterior interosseous nerve. Electrical neural stimulations were delivered during the MVC (after a plateau of 1 s) by a high-voltage stimulator (Digitimer DS7AH, Digitimer, Welwyn Garden City, UK). Each twitch duration was 0.2 ms, the tension was 400 V, and the amperage stimulation was determined for each subject during the familiarisation session as 1.2 x the amperage needed to obtain a maximal muscle action potential (M-wave). The cathode was positioned proximally and the anode distally over the posterior interosseous nerve, with an inter-electrode distance of 3 cm. During the other three MVC the motor cortex was further activated by TMS. Motor evoked potentials (MEP) were elicited via a circular coil (13.5 cm outside diameter) positioned over the vertex and connected to a single twitch magnetic stimulator (Magstim 200, Whitland, UK). The direction of the current in the coil was chosen to activate the motor cortex in the hemisphere that innervated the right arm. The stimulator output was calculated by multiplying the value of threshold by 1.2 for each subject and was readjusted before each trial. The electromyographic (EMG) signal was recorded on the abductor pollicis longus using MP35 hardware (Biopac Systems, Santa Barbara, CA) and dedicated software (BSL Pro Version 3.6.7, Biopac Systems). Surface EMG was recorded from the muscle belly using bipolar Ag/AgCl disposable electrodes (Ambu Blue sensor T, Ballerup, Denmark) with a diameter of 9 mm and an interelectrode distance of 3 cm. The ground electrode was placed on the right wrist. Before electrode placement the skin was lightly abraded and washed to remove surface layers of dead skin, hair, and oil. The myoelectric signal was amplified and filtered (band pass 30–500 Hz, gain ¼ 1000), and the frequency of data collection was 2000 Hz. The root mean square (RMS) of the EMG activity was recorded during each MVC over a 1 s period, before the superimposed evoked potential. The amplitude of the superimposed M-wave was used to calculate the RMS/M and MEP/M ratio during MVC. The duration of the silent period following MEP was also measured. Statistical analysis Data was coded and analysed in SPSS Version 17 software (Chicago, IL) and represented as mean # SEM. A two-way within subjects ANOVA


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with repeated measures was performed to assess the effect of time, condition and the potential interaction. In the HOT condition, pairwise t-tests were used to assess changes in body temperatures recorded at the start and end of each cognitive trial. Data was screened for outliers, normality and homogeneity of variance using the Fmax test. Whenever outcome variables displayed departure from normality, logarithmic transformations were applied. All variables were tested using Mauchly’s test for sphericity. Whenever the data violated the assumption of sphericity a p-value based on lower bound correction was reported. If a significant time ' condition interaction was found, pairwise comparisons using a Bonferroni correction was used to compare the effect of condition upon time. The level of statistical significance was set at p50.05. Results Temperatures There were global effects of time (all, F1,7410.4, p50.014, effect size (ES)40.6) and condition (all F1,74126.1, p50.001, ES40.95), as well as the interaction (all F3,21426.1, p50.001, ES40.82) for Tcore and Tchest. For Thand there were significant effects of condition (F1,7 ¼ 1058, p50.001, ES ¼ 0.99) and the interaction between condition and time (F3,21 ¼ 42.6, p50.001, ES ¼ 0.86). Figure 1 shows that Tcore, Tchest and Thand (all, P50.001) were significantly higher in HOT than CON at ALL time points except at T1 in the case of Tcore. Pairwise comparison revealed that there was a significant difference in the Tcore start and end of the cognitive trial only at T4 (P ¼ 0.004) (Figure 2). Whereas there was a significant increase in Tskin only at T1 (p50.003, Figure 1). Cognitive functions The OTS-4 did not show any significant effect of condition (F1,6 ¼ 1, NS, Figure 3), time or any interaction effects (all F3,1850.4, NS, Figure 2). The OTS-6 did not show a time effect (F3,18 ¼ 0.4, NS) but was significantly lower in HOT than in CON (F1,6 ¼ 61.2, P50.001, ES ¼ 0.91) and displayed an interaction effect (F3,18 ¼ 3.5, p ¼ 0.036, ES ¼ 0.7). Post hoc analysis revealed significantly lower OTS-6 scores at T1 (P ¼ 0.05) and T4 (P ¼ 0.006) in HOT compared to CON (Figure 2). Neuromuscular testing Maximal force production (Figure 3) was not globally dependent on time (F1,7 ¼ 0.3, NS), but was significantly lower in HOT as compared to CON (F1,7 ¼ 6.1, P ¼ 0.043, ES ¼ 0.47). This decrement

was dependent upon exposure time (F3,21 ¼ 7.2, P ¼ 0.002, ES ¼ 0.51), becoming significant from T2 onwards (all, P50.05). RMS/M ratio (Figure 3) was reduced in HOT as compared to CON (F1,7 ¼ 9.4, P ¼ 0.015, ES ¼ 0.61) with an effect of time (F3,18 ¼ 3.2, P ¼ 0.049, ES ¼ 0.35) without an interaction effect (F3,21 ¼ 2.2, NS). The MEP/M was not globally dependent on time (F3,21 ¼ 1.7, NS) but was significantly lower in HOT than CON (F1,7 ¼ 9.5, P ¼ 0.018, ES ¼ 0.58, Figure 3) and displayed an interaction effect (F3,21 ¼ 6.4, P ¼ 0.003, ES ¼ 0.48). Post hoc analysis revealed that the difference between conditions significantly increased from T3 onwards (both, P50.016). An example of the MEP wave is displayed in Figure 4. There were no global effects of condition (F1,7 ¼ 2.7, NS) or time (F3,21 ¼ 1.0, NS) on the MEP silent period (64.8 # 6.6 ms). There was a global effect of condition (F1,7 ¼ 9.5, P ¼ 0.018, ES ¼ 0.58) but no effect of time (F3,21 ¼ 2.9, NS) on M-wave amplitude (8.0 # 1.2 mV). Discussion The aim of this study was to investigate the changes in neuromuscular and cognitive functions occurring during passive heat exposure. Data revealed that at the onset of heat exposure, with a normothermic Tcore decrements occurred in OTS-6 planning task suggesting that complex cognitive performance can be affected by rapid changes in environmental temperature. Although index of motor cortical excitability deteriorated with the increase in Tcore, complex cognitive performance recovered. However, when Tcore reached 38.8" C (i.e. hyperthermia), both complex cognitive performance and neuromuscular functions were altered. Only Tskin increased upon entering the environmental chamber in the HOT condition (Figure 1), suggesting Tskin is more responsive to the environmental stimuli than to an increase in Tcore [25]. Interestingly, even in the absence of motor cortical excitability alterations (i.e. MEP/M ratio), OTS-6 was altered immediately upon entering the climate chamber, presumably in response to the sudden change in environmental conditions. Within 10 min of first entering the environmental chamber the first cognitive trial was completed, which corresponded with an increase in Tskin with Thand and Tchest increasing by $3.3" and 2" C, respectively (Figure 1). The sensitivity of cognitive function to changes in Tskin could be partly related to the feelings of pleasure or displeasure that they induce (alliesthesial effect [26]). Pleasurable thermal stimuli return the body to its homoeostatic state, while unpleasurable



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Figure 1. Core, chest and hand temperatures during a trial (left panel) in neutral (CON, dashed line) and hot (HOT, plain line) environments as well as during the cognitive testing of the different sessions (T1, T2, T3, T4) in hot condition (right panel). Values in Mean # SEM. *Significant differences between conditions; $significant increase during the cognitive testing, p50.05.

thermal stimuli take the body away from it [27]. Therefore, the increase in Tskin observed at the onset of heat exposure generated unpleasant stimuli that could be considered as a ‘cognitive load’. This load places additional attentional demands on a limited workspace [28], reducing the available resources for concurrent (cognitive) tasks. Cooling the head has been shown to restore complex cognitive function in a hot environment possibly by reducing the load [16]. In this experiment, the OTS-4 required lower cognitive resources than the OTS-6, and consequently, despite the additional cognitive load coming from the rapid increase in Tskin upon heat exposure,

there were sufficient resources to successfully complete the task. At T2 and T3, Tcore increased to 37.8" C and 38.3" C respectively, but there were no alterations in cognitive performance at both levels of OTS complexity (Figure 2). Although Tskin significantly increased from T1 there was no variation in Tskin within either the T2 or T3 cognitive trial (Figure 1). This finding suggests the importance of the rate of change in Tskin on cognitive function rather than the absolute temperature per se. However, voluntary force production was lower in HOT than in CON at both time-points (Figure 3), suggesting that force


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Figure 2. Number of problems solved on the first choice during the OTS (One Touch Stockings of Cambridge). Data in neutral control (CON, white bars) and hot (HOT, black bars) environments for two different levels of difficulty (OTS-4, top graph; OTS-6, bottom graph), at 4 different sessions (T1, T2, T3, T4). Values in Mean # SEM. *Significant differences between conditions, p50.05.

production was not influenced by variations in Tskin but is sensitive to increases in Tcore [15]. As with other studies [14, 15], the current data demonstrate that voluntary force production can be decreased with a relatively moderate elevation in Tcore ($38" C). In addition, the global decreases in RMS/M ratio (Figure 3) suggest this decrement in force production can be partly linked to a reduction in muscle neural drive. This reduction in RMS/M is a novel observation during passive heat exposure and supports the decrements previously reported in voluntary muscle activation with hyperthermia [14–16]. Interestingly, the alterations in force production and neural drive were only accompanied by a decrement in the MEP/M ratio at a Tcore of 38.3" C. This suggests that the impairment in RMS/M with moderately elevated Tcore (i.e. 37.8" C) during heat exposure could partly originate from outside the motor cortex.

A decrement in force production could be linked to any stage between the subject’s motivation and the muscle contractile properties. Hyperthermia has previously been shown to reduce sarcolemmal excitability [16]. However, the absence of variation in M-wave amplitude and the decrement in RMS/M and MEP/M ratio in the current study suggests the existence of alterations in the central nervous system (CNS). The CNS is under influence of peripheral afferents; for example, group III and IV afferents increase their firing rate when exposed to hot temperatures [29, 30]. In the current study, inhibition mediated by group III and IV afferents could reduce the RMS/M and MEP/M via a spinal modulation of the descending neural drive due to hyperthermia [16]. However, these afferents may not directly inhibit motoneurons but could act on other brain areas activating the motor cortex (upstream) [31]. In the current experiment,

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Figure 3. Neuromuscular responses in neutral (CON, dashed line) and hot (HOT, plain line) environments at 4 different sessions (T1, T2, T3, T4). Maximal voluntary force displayed an interaction effect with significantly lower values in HOT than CON in T2, T3 and T4. Normalised (RMS/M) muscle electrical activity was globally lower in HOT than CON. The amplitude of the motor-evoked potential normalised by the amplitude of M-wave (MEP/M) displayed an interaction effect with significantly lower values in HOT than CON in T3 and T4. Values in Mean # SEM. *Significant differences between conditions, p50.05.


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Figure 4. Example of motor evoked potential (MEP) by transcranial magnetic stimulation (TMS) for one subject. Curves represent the average of 3 MEP recorded during the fourth test session (T4) in neutral (plain line) and hot (dashed line) environment.

magnetically evoked indices of neural drive (i.e. MEP/M) were not altered, but when Tcore was below $38" C (T2) decrements in voluntary force production and neural drive (i.e. RMS/M) were observed. Taken together, these results suggest the existence of a limitation upstream of the motor cortex for maximal muscle activation in hot environments. Although, no electro encephalogram (EEG) was recorded in this experiment to support this hypothesis, the perturbation in cognitive function observed upon heat exposure in the absence of MEP/M alterations confirms that other brain functions (e.g. motivation) are altered in hot environments. After 4 h 30 min of heat exposure, Tcore further increased to 38.8" C. At this absolute Tcore, both complex cognitive task (OTS-6, Figure 2) and neurophysiological (Force, RMS/M, MEP/M, Figure 3) functions were significantly impaired. The alteration in cortical excitability (i.e. MEP/M) could be considered detrimental to cognitive function. However, our data showed that motor cortical excitability was impaired from 38.3" C without cognitive alterations, which suggest that different triggers were involved in the deterioration of cognitive and physiological functions. Cognitive performance has been suggested to decrease when environmental conditions induce a dynamic and non-compensatable change in Tcore [20]. Therefore, we suggest that the cognitive alterations observed during this trial could originate from the interference between the additional load imposed by the dynamic changes in Tcore observed during T4 and the cognitive task itself. This was confirmed by the absence of adverse effects of hyperthermia on the OTS-4, which requires fewer cognitive resources to be successfully completed. As suggested by Hocking et al. [4],

performance in cognitive tasks deteriorates when the total cognitive resources are insufficient for both the task and the thermal stress (interfering load). This hypothesis is partly supported by neurophysiological imaging studies showing the greater use of neural resources (initial increase in electrical activity) to maintain the same cognitive performance in a hot environment [32] until the resources are overloaded [4], at which time cortical activity may decrease [33]. However, the relative influence of the high Tcore per se and its dynamic changes cannot be determined in the current study, which did not include a hyperthermic trial without a dynamic change in Tcore. Interference has previously been observed between two concurrent cognitive tasks [34–38], two motor tasks [39–41], the combination of a cognitive and a motor task [42–46], and during exercise-induced fatigue in a hot environment [32]. In addition, interference has been suggested to reduce cognitive performance when two concurrent tasks involved overlapping areas of the cerebral cortex [47]. In the current experiment the OTS task provides a measure of frontal lobe functioning [48], which corresponds to the area of the brain affected by hyperthermia [49, 50]. Therefore, we suggest that passive heat exposure could also interfere with the cognitive processes and could be studied using the double task paradigm. Conclusion The increase in Tcore limits force production capacity possibly via alterations occurring upstream of the motor cortex (from Tcore $ 37.8" C) but also via a decrement in motor cortical excitability (from Tcore $ 38.3" C). These alterations in cortex

Cognitive and neuromuscular alterations excitability failed to explain the deterioration in complex cognitive performance. Therefore, we suggest that the cognitive load imposed by the rapid increase in Tskin or Tcore caused performance decrements in complex cognitive task. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.


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