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Using a Combination of Indirect Calorimetry, Infrared Thermography, and Blood Glucose Levels to Measure Brown Adipose Tissue Thermogenesis in Humans

In mammals, brown adipose tissue (BAT) is activated rapidly in response to cold in order to maintain body temperature. Although BAT has been studied ...

La Trobe University

The University of Melbourne

The study of human bioscience is viewed as a crucial curriculum in allied health. Nevertheless, bioscience (and particularly physiology) is notoriously difficult for undergraduates, particularly academically disadvantaged students. So endemic are the high failure rates (particularly in nursing) that it has come to be known as "the human bioscience problem." In the present report, we describe the outcomes for individual success in studying first-year human physiology in a subject that emphasises team-based active learning as the major pedagogy for mastering subject learning outcomes. Structural equation modeling was used to develop a model of the impact team learning had on individual performance. Modeling was consistent with the idea that students with similar academic abilities (as determined by tertiary entrance rank) were advantaged (scored higher on individual assessment items) by working in strong teams (teams that scored higher in team-based assessments). Analysis of covariance revealed that students who studied the subject with active learning as the major mode of learning activities outperformed students who studied the subject using the traditional didactic teaching format (lectures and tutorials, P = 0.000). After adjustment for tertiary entrance rank (via analysis of covariance) on two individual tests (the final exam and a late-semester in-class test), individual student grades improved by 8% (95% confidence interval: 6-10%) and 12% (95% confidence interval: 10-14%) when students engaged in team-based active learning. These data quantitatively support the notion that weaker students working in strong teams can overcome their educational disadvantages.

The use of team-based, guided inquiry learning to overcome educational disadvantages in learning human physiology: a structural equation model.

Evidence shows that factors contributing to success in physiology education for allied health students at universities include not only their high school achievement and background but also factors such as confidence with their teachers and quality of their learning experience, justifying intensive and continued survey of students' perceptions of their learning experience. Here we report data covering a 3-yr period in a physiology subject that has been redesigned for blended and online presentation. Consistent with previous reports, we show that when we undertook a blended mode of delivery, students demonstrated better grades than traditional modes of teaching; however the absence of didactic teaching in this subject resulted in lower grades overall. Students have very strong positive attitudes to weekly quizzes (80% positive approval) but report ambivalent attitudes to online self-directed learning (61% negative perception), even though they had 2-h weekly facilitated workshops. Overwhelmingly, students who undertook the subject in a self-directed online learning mode requested more face-to-face-teaching (70% of comments). From these data, we suggest that there is a quantifiable benefit to didactic teaching in the blended teaching mode that is not reproduced in online self-directed learning, even when face-to-face guided inquiry-based learning is embedded in the subject.

Student perceptions and learning outcomes of blended learning in a massive first-year core physiology for allied health subjects.

"Only teach me what I need to know!" This commonly heard refrain is often spoken by allied health students while studying preclinical sciences (physiology, anatomy, pharmacology). Here we use a clinical scenario undertaken by second-year Bachelor of Paramedic Practice students of acute coronary syndrome to demonstrate the difference in clinical decision making when using a clinical reasoning approach to treatment rather than relying exclusively on a practice guidelines approach. We hope to demonstrate that understanding basic bioscience concepts, such as the Frank-Starling mechanism and the anatomy and physiology of the autonomic nervous system, are key to providing good clinical care in response to ambiguous patient symptoms. Students who understand these concepts underlying their patient care guideline will make better clinical decisions and better provide quality of care than students who follow the guideline exclusively. We aim this as a practical demonstration of the value of detailed understanding of human bioscience in allied health education. As health care providers transition from "technician" to "practitioner," the key distinguishing feature of the role is the ability to practice independently, using "best judgment" rather than clinical guidelines (alone). Evidence suggests that complex case management requires detailed bioscience understanding.

The difference between a clinical technician and clinical practitioner is in the scope of practice: the need for a bioscience understanding in paramedicine.

Pharmacological interventions to aid weight loss have historically targeted either appetite suppression or increased metabolic rate. Brown adipose tissue (BAT) possesses the capacity to expend energy in a futile cycle, thus increasing basal metabolic rate. In animal models, oestrogen has been implicated in the regulation of body weight, and it is hypothesized that oestrogen is acting by modulating BAT metabolism. A systematic search was performed, to identify research articles implementing in vivo oestrogen-related interventions and reporting outcome measures that provide direct or indirect measures of BAT metabolism. Meta-analyses were conducted where sufficient data were available. The final library of 67 articles were predominantly in rodent models and provided mostly indirect measures of BAT metabolism. Results of this review found that oestrogen's effects on body weight, in rats and possibly mice, are likely facilitated by both metabolic and appetitive mechanisms but are largely only found in ovariectomized models. There is a need for further studies to clarify the potential effects of oestrogen on BAT metabolism in gonad-intact and castrated male animal models.

The capacity for oestrogen to influence obesity through brown adipose tissue thermogenesis in animal models: A systematic review and meta-analysis.

Functional brown adipose tissue (BAT) was identified in adult humans only in 2007 with the use of fluorodeoxyglucose positron emission tomography imaging. Previous studies have demonstrated a negative correlation between obesity and BAT presence in humans. It is proposed that BAT possesses the capacity to increase metabolism and aid weight loss. In rodents it is well established that BAT is stimulated by the sympathetic nervous system with the interscapular BAT being innervated via branches of intercostal nerves. Whilst there is evidence to suggest that BAT possesses beta-3 adrenoceptors, no studies have identified the specific nerve branch that carries sympathetic innervation to BAT in humans. The aim of this study was to identify and trace the peripheral nerve or nerves that innervate human BAT in the supraclavicular region. The posterior triangle region of the neck of cadaveric specimens were dissected in order to identify any peripheral nerve branches piercing and/or terminating in supraclavicular BAT. A previously undescribed branch of the cervical plexus terminating in a supraclavicular adipose depot was identified in all specimens. This was typically an independent branch of the plexus, from the third cervical spinal nerve, but in one specimen was a branch of the supraclavicular nerve. Histological analysis revealed the supraclavicular adipose depot contained tyrosine hydroxylase immunoreactive structures, which likely represent sympathetic axons. This is the first study that identifies a nerve branch to supraclavicular BAT-like tissue. This finding opens new avenues for the investigation of neural regulation of fat metabolism in humans.

Innervation of supraclavicular adipose tissue: A human cadaveric study.

The impact of brown adipose tissue (BAT) metabolism on understanding energy balance in humans is a relatively new and exciting field of research. The pathogenesis of obesity can be largely explained by an imbalance between caloric intake and energy expenditure, but the underlying mechanisms are far more complex. Traditional non-selective sympathetic activators have been used to artificially elevate energy utilization, or suppress appetite, however undesirable side effects are apparent with the use of these pharmacological interventions. Understanding the role of BAT, in relation to human energy homeostasis has the potential to dramatically offset the energy imbalance associated with obesity. This review discusses paradoxical effects of caffeine on peripheral adenosine receptors and the possible role of adenosine in increasing metabolism is highlighted, with consideration to the potential of central rather than peripheral mechanisms for caffeine mediated BAT thermogenesis and energy expenditure. Research on the complex physiology of adipose tissue, the embryonic lineage and function of the different types of adipocytes is summarized. In addition, the effect of BAT on overall human metabolism and the extent of the associated increase in energy expenditure are discussed. The controversy surrounding the primary β-adrenoceptor involved in human BAT activation is examined, and suggestions as to the lack of translational findings from animal to human physiology and human  to  models are provided. This review compares and distinguishes human and rodent BAT effects, thus developing an understanding of human BAT thermogenesis to aid lifestyle interventions targeting obesity and metabolic syndrome. The focus of this review is on the effect of BAT thermogenesis on overall metabolism, and the potential therapeutic effects of caffeine in increasing metabolism via its effects on BAT.

Effects of Caffeine on Brown Adipose Tissue Thermogenesis and Metabolic Homeostasis: A Review.

Using a combination of respiratory gas exchange, infrared thermography, and blood glucose (BGL) analysis, we have investigated the impact of  fruit powder (475 mg) or caffeine (100 mg) on metabolic activity in a placebo controlled (lactose, 100 mg) double-blinded three-way cross-over-design experiment. Metabolic measurements were made on day 1 and day 7 of supplementation in eight adult male participants (22.2 ± 2 years of age, BMI 23 ± 2 kg/m, x̅ ± SD). Participants arrived fasted overnight and were fed a high carbohydrate meal (90 g glucose), raising BGL from fasting baseline (4.4 ± 0.3 mmol/L) to peak BGL (8.5 ± 0.3 mmol/L) 45 min after the meal. Participants consumed the supplement 45 min after the meal, and both caffeine and  fruit powder restored BGL (F  = 2.2,  = 0.02) to near fasting levels within 15 min of supplementation compared to placebo (120 min). In parallel both supplements increased energy expenditure (F  = 175.6,  < 0.001) over the 120-min test period (caffeine = 50.74 ± 2 kcal/kg/min,  fruit = 50.95 ± 1 kcal/kg/min, placebo = 29.34 ± 1 kcal/kg/min). Both caffeine and  fruit powder increased supraclavicular fossa temperature (F  = 32,  < 0.001) on both day 1 and day 7 of testing over the 120-min test period. No statistical difference in core temperature or reference point temperature, mean arterial pressure or heart rate was observed due to supplementation nor was any statistical difference seen between day 1 and day 7 of intervention. This is important for implementing dietary ingredients as potential metabolism increasing supplements. Together the results imply that through dietary supplements such as caffeine and , mechanisms for increasing metabolism can be potentially targeted to improve metabolic homeostasis in people.

Both caffeine and  fruit powder lower blood glucose levels and increase brown adipose tissue temperature in healthy adult males.

[This corrects the article DOI: 10.3389/fphys.2022.870154.].

Article	Year
The use of team-based, guided inquiry learning to overcome educational disadvantages in learning human physiology: a structural equation model. Advances in physiology education\| PubMed ID: 25179611	2014
Student perceptions and learning outcomes of blended learning in a massive first-year core physiology for allied health subjects. Advances in physiology education\| PubMed ID: 28143822	2017
The difference between a clinical technician and clinical practitioner is in the scope of practice: the need for a bioscience understanding in paramedicine. Advances in physiology education\| PubMed ID: 31697166	2019
The capacity for oestrogen to influence obesity through brown adipose tissue thermogenesis in animal models: A systematic review and meta-analysis. Obesity science & practice\| PubMed ID: 31890250	2019
Innervation of supraclavicular adipose tissue: A human cadaveric study. PloS one\| PubMed ID: 32702004	2020
Effects of Caffeine on Brown Adipose Tissue Thermogenesis and Metabolic Homeostasis: A Review. Frontiers in neuroscience\| PubMed ID: 33613184	2021
Both caffeine and fruit powder lower blood glucose levels and increase brown adipose tissue temperature in healthy adult males. Frontiers in physiology\| PubMed ID: 36017333	2022
Corrigendum: Both caffeine and fruit powder lower blood glucose levels and increase brown adipose tissue temperature in healthy adult males. Frontiers in physiology\| PubMed ID: 36703937	2022

Joseph A. Rathner

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