External force to live long and prosper: A passive exercise classification framework

Highlights

• •A standardized definition for “passive exercise” has not been adopted in the current literature.
• •We provide an operational definition of passive exercise as planned, structured, and repetitive passive movements designed to promote specific physical, cognitive, or health outcomes.
• •We identify passive exercise modalities that might facilitate more cost-effective and individually tailored interventions supporting brain health.
• •We explain how passive exercise differs from passive movement and that passive exercise can be further classified into distinct categories.

1. Introduction

Passive movement is a 200+ year-old manipulation involving the external movement of an individuals’ limbs or body absent voluntary effort or muscle contraction.¹ The original application of passive movement was therapist-guided limb manipulation to increase range of motion and blood supply following acute and chronic injury. Beyond physical rehabilitation, passive movement has been identified as a potential means to support cognitive and brain health.2, 3, 4, 5, 6, 7, 8, 9, 10, 11 Notably, however, the current literature does not provide an operational distinction between “passive movement” and “passive exercise”, and the terms have frequently been used as interchangeable.¹ The above-cited studies have made use of a variety of techniques including whole-body vibration (WBV), muscle pump stimulation, and motorized cycling. WBV typically involves standing on a platform that transmits repetitive vibrations to the body (e.g., 20–60 Hz3, 4, 5) and renders rapid and involuntary contractions to the leg and/or postural muscles.3, 4, 5 In turn, muscle pump stimulation involves the passive activation of relaxed muscles. For example, micromechanical stimulation of the soles of the feet which activates a lower-limb postural reflex arc and engenders the contraction and relaxation of the soleus muscle.⁶ Last, motorized cycling involves the rhythmic cycling of participants’ upper- or lower- limbs via a mechanically driven flywheel that can engage the same range of motion and movement frequency, and duration as “active” aerobic cycling.^2,7, 8, 9, 10, 11 The use of several passive modalities is salient given that modality-specific changes at the level of the manipulated muscle, as well as whole-body cascades, are likely to modulate the degree to which such movement influences the brain.

To advance the field of exercise neuroscience and better understand the relationship between passive movement and brain health, a clear classification framework is required. This opinion piece will therefore argue for the distinct classification of passive modalities based on the oft-cited Frequency, Intensity, Time, Type, Volume, Progression (FITT-VP) framework that is used to distinguish between physical activity and physical exercise.¹² Accordingly, the below will argue that modalities should be classified as either “passive movement” (i.e., muscle pump stimulation), and “passive exercise”. We aimed to outline why the latter should be used to refer to the planned, structured, and repetitive form of passive movement designed to promote specific physical, cognitive, or mental health outcome (Fig. 1). Furthermore, we propose a distinction between static exercises (i.e., WBV) and those that involve cyclical and purposeful movements that mimic active exercise and occur at a frequency comparable to active exercise. We will outline works describing the neurophysiological responses to different forms of passive movement before providing a rationale for our distinction. We hope that our proposed framework serves to facilitate future recommendations to better support brain health.¹³

Fig. 1.

A graphical representation of why and how a classification framework will support future research investigating passive exercise. FITT-VP = Frequency, Intensity, Time, Type, Volume, Progression.

2. Current state of evidence on passive exercise and cognitive health

2.1. Passive cycling

As it is beyond the scope of this viewpoint to discuss the history and the documented physiological responses of passive movement-related research, we encourage the reader to consult Trinity and Richardson’s¹ review for a more detailed overview. Instead, we focus on cognitive changes and neurophysiological responses associated with different types of passive movement as a relevant and emerging line of research.¹³ In particular, we begin by outlining work by James Duffin’s group14, 15, 16 which characterised changes in cardiorespiratory fitness and cerebral haemodynamic alterations associated with a single bout of passive cycling and then describe work relating to passive exercise-induced changes in cognition and executive function. It is here we would like to propose that the type of passive modality undertaken will modulate physiological and cognitive outcomes. First, Bell and colleagues¹⁴ compared the effects of 5-min of passive cycling via tandem cycle (i.e., movement of the experimenter’s lower limbs propelled the lower limbs of the participant) and a tandem seated leg extension chair (i.e., extension of the experimenter’s lower limbs propelled the lower limbs of the participant). The authors demonstrated that passive cycling produced a more rapid exercise drive to breathe compared to the passive leg extension condition and that this response was associated with increased ventilation, CO₂ production, O₂ consumption, and the drive to breathe deeply.¹⁵ Accordingly, it was concluded that the passive modality (i.e., cycling vs. leg extension) directly affects the neural and metabolic processes that influence physiological homeostasis in response to external movement, and highlights the need to differentiate between passive exercise modalities. Furthermore, the type of passive movement (e.g., supine motorised passive cycling)¹⁶ such as the passive repetitive flexion and extension of the upper and lower limbs¹⁷ has been shown to influence the degree to which cerebral blood flow (CBF) is modulated. This is particularly important given that previous work has demonstrated a link between changes to CBF and improved cognition in healthy¹⁸ and clinical^2,19 populations. Passive cycle ergometry leads to the activation of mechanosensitive group III muscle afferents,²⁰ feedforward command mechanisms,²¹ and baroreflex activation²² that stimulate the primary somatosensory and motor cortices to increase cardiac output and stroke volume and ultimately leads to an increase in CBFa.^20,23

It is accepted that healthy individuals, and those with chronic illnesses, benefit from bouts of active exercise (i.e., volitional movement of the limbs).¹⁹ However, individuals with limited mobility (e.g., Parkinson’s disease, stroke, spinal cord injury, coma) may experience challenges or be unable to complete prescribed regimens of active exercise for various reasons (e.g., low exercise tolerance with more negative affective response, lack of motivation or inability to perform active exercise). Accordingly, Ridgel and colleagues² had persons with Parkinson’s disease complete single 30-min bouts of passive lower limb cycling at 60, 70, and 80 revolutions per minute (rpm) and measured pre- and post-passive exercise executive function (i.e., a high-level cognitive construct) via the Trail-Making Test (TMT). Results showed a pre- to post-exercise improvement in executive function that the authors attributed to a passive cycle-induced increase in CBFb. Subsequent work by our group has demonstrated that (a) an increase in CBF independent of movement (i.e., via inhalation of a higher-than-atmospheric concentration of CO₂) is sufficient to improve executive function;¹⁸ and (b) that passive exercise reliably elevates CBF and is associated with an executive function benefit.^7,8 Together, this corpus of work provides evidence that passive cycling benefits cognition in healthy young adults and those with a chronic illness.

2.2. Muscle pump stimulation and WBV

In line with passive cycle ergometry, other passive movement modalities have shown executive function benefits following chronic implementation. First, McLeod and Stromhaug’s⁶ pilot investigation examined the effects of a passive calf muscle pump stimulation (via electrical activation of the soleus muscle reflex arc) on a small sample (n = 5) of older adults (mean age = 82.5 years) with chronic hypertension. Participants’ blood pressure and executive function (via the Stroop task and TMT) were monitored during a 4-month intervention period that included a daily 60-min-long calf muscle stimulation intervention. Results demonstrated normalized (i.e., becoming similar to healthy controls) diastolic blood pressure, with no change to systolic blood pressure, and improved executive function.⁶ It is, however, important to recognize that this work did not employ an appropriate control condition or a control group, and given that the Stroop task and TMT are associated with learning effects,24, 25, 26, 27 the improved task performance cannot be directly attributed to the muscle-pump stimulation protocol. As well, Regterschot and colleagues³ investigated the effects of passive WBV on 133 healthy young adults. Participants underwent six 2-min WBV sessions and six 2-min sessions of rest with each session followed by an executive function assessment via the Stroop and backward digit span tasks. Results demonstrated that WBV selectively improved performance on the color-word version of the Stroop task. In turn, performance on the backward digit span task was not affected by WBV. Single and repeated bouts of WBV have generally been shown to benefit cognition in children and adults,^4,5 and its use in the context of dementia care is also being explored.²⁸ These results should be taken with caution because the degree to which WBV benefits cognition might relate to task-specific outcomes (e.g., order and time of task presentation, task practice effects in a repeated measures design) rather than the modality itselfc. Animal studies provide some mechanistic insight into how WBV and muscle pump stimulation might support cognition/executive function by demonstrating that sensory stimulation-related alterations to neurotransmission in higher-order and memory-related brain regions support this benefit.^3,29,30

In the studies described in the previous paragraphs (i.e., cycling, muscle-pump, WBV) all authors refer to their manipulations as “passive exercise” thus illustrating the heterogeneity by which the term is used. Accordingly, we contend that passive exercise should be further classified and operatically defined because it will allow for a nuanced understanding of the different candidate neurobiological mechanisms supporting brain health in healthy individuals and those with a chronic illness.

3. A Classification framework/approach for passive exercise

A classification framework, which is currently absent from the literature, will help to guide future research. Thus, based on the established framework for active physical exercise (i.e., the FITT-VP principle¹²), we propose the following framework for passive exercise (Table 1) wherein muscle pump stimulation is classified as passive movement and WBV and passive cycling (upper and lower limb) should be classified as “categories” of passive exercise. Indeed, the need for a more fine-grained differentiation between different types of passive exercise becomes clearer when contrasting between WBV and passive cycle ergometry. For example, although both types of passive movements are induced by external forces, neither WBV nor passive cycle ergometry induce a marked expenditure of energy, but the former elicits a smaller increase (e.g., <0.5 kcal/min and <1.23 kcal/min increase from rest during WBV and passive cycling, respectively).^31,32 Additionally, WBV does not entail cyclical and purposeful movements that induce the lengthening of agonist and antagonist muscles at a frequency on par to active exercise and providing a range of motion associated with locomotor-based activities of daily living.³³ Indeed, passive cycling involves the progressive and cyclic shortening and lengthening of muscle fibres, and this rhythmic activity has been shown to elicit alterations in muscle oxygenation, blood flow, and a central cardiovascular response³³ that is associated with an increase in CBF.²⁰ In contrast, WBV does not elicit cyclic movement patterns and renders only very small changes in muscle length and tension in agonist and antagonist musculature.³⁴ Accordingly, as it seems reasonable to assume that passive cycling might be more effective to improve specific health outcomes (e.g., brain health) compared to WBV, we propose that passive cycling should therefore be classified as a first type passive exercise, whereas WBV should be classified as a second type “static” passive exercise. More research is of course needed to empirically assess this assumption.

Table 1.

Overview of selected exercise characteristics that should be considered when determining the dosage of passive exercise.

Variable	Description
Frequency	… the number of passive exercise bouts in a specific time interval (e.g., session, day, week, or year).
Intensity	… the external force applied for passive exercise (i.e., external load operationalized by rpm of the flywheel) and psychophysiological reaction to it (i.e., internal load such as ratings of perceived exertion, heart rate, cerebral blood flow). Currently, the intensity of passive exercise is typically provided via external load, but we recommend that future studies (a) report both external load and internal load, or (b) report, in the optimal case, individual adjustments to the external load to achieve comparable internal load.
Time	… the time spent for a specific type of passive exercise, a passive exercise training session, or a passive exercise intervention.
Type	… the kind of passive exercise conducted in a passive exercise training session. In this context, we recommend defining the type of passive exercise according to the key characteristics of (a) how the external force is delivered (i.e., via a device or physiotherapist); (b) the limbs manipulated (i.e., upper, lower, or whole body); (c) the modes of stimulation (i.e., continuous versus interval, or cyclic versus acyclic); and (d) presence or absence of joint movements (i.e., static with little-to-no movement or dynamic across an appreciable range of motion).
Density	… the timing of passive exercise within a specific interval by specifying the rest (recovery) duration between two consecutive bouts of passive exercise.
Volume	…defines the total amount of passive exercise that is conducted in a specific period (i.e., volume = frequency × time).
Progression	…defines how a passive exercise regimen should be progressed/advanced over time by purposefully adjusting the exercise variables (e.g., increasing intensity, duration or frequency).

Notes: We emphasize that the exact determination of the dose of passive exercise is complex (e.g., comparable to active physical exercise)^39,40 and therefore recommend adhering to established guidelines for reporting the characteristics of active physical exercise in addition to those already provided here (e.g., CERT)⁴¹. Although not in the original FITT-VP framework, we include density here for additional clarity when applying passive exercise to future work.^39,40 In future, standardization of passive exercise regimens should include guidelines for how intensity is quantified, as well as the way in which external forces are imparted to participants’ limbs and bodies.

Abbreviations: CERT = consensus on exercise reporting template; FITT-VP = Frequency, Intensity, Time, Type, Volume, Progression; rpm = revolutions per minute.

The intentionally broad definition of “passive movement” and the tendency for this term to be used interchangeably with “passive exercise”¹ can be a source of confusion in scientific communications which aim to avoid ambiguity. Thus, based on the conceptual differences that have been established for “physical activity” and “physical exercise”,³⁵ we propose that a comparable differentiation should be applied to “passive movement” and “passive exercise” (Table 1 and Appendix). This differentiation will allow for unambiguous communication in future scientific practice. Such an explicit differentiation between these terms will not only allow for clearer communication, but also for the more efficient translation of established frameworks for active physical exercise prescription (e.g., FITT-VP) to the field of passive exercise.

4. Implications and conclusion

The current definition of passive movement is intentionally broad to encompass a wide range of techniques meant to study the body’s responses to altered homeostasis, as well as injury recovery and health promotion. As interest in this research field is growing, especially on the effects of passive exercise on cognition and executive function,¹³ we emphasize that the term “passive exercise” should be applied to planned, structured, and repetitive forms of passive movement.

Such a clear classification method for this modality will positively influence scientific advancement, clinical practice, and public policy. For example, a clear understanding of what constitutes passive exercise can be used to appropriately define underlying mechanisms responsible for cognitive improvements in healthy individuals and persons with chronic disease. Moreover, understanding how to successfully implement and precisely dose passive exercise will improve health equality and subsequently contribute to a reduction in the healthcare burdens, particularly for those with physical limitations. The results of these works can then be used to shape public health guidelines to benefit the wider population. Therefore, we propose in this article the implementation of a classification framework for passive exercise which hopefully will facilitate innovative research to improve clinical outcomes and shape guidelines for the application of this exercise modality.

Authors’ contributions

BT conceptualized the idea of this manuscript and drafted the initial version; MH, FH and LZ conceptualized the idea of this manuscript; YBW and QY contributed to subsequent versions of the manuscript. All authors have edited and provided feedback which shaped the manuscript. All authors have read and approved the final version of the manuscript, and agree with the order of presentation of the authors.

Competing interests

The authors declare that they have no competing interests.

Appendix. Infobox: “only logical” to differentiate passive movement and passive exercise

We propose that the terms passive movement and passive exercise can be differentiated using the criteria that are applied to distinguish between physical activity and physical exercise. Physical activity is typically defined as “any bodily movement produced by skeletal muscles that results in energy expenditure”³⁵ above 1.5 metabolic equivalents (MET),³⁶ whereas physical exercise refers to planned, structured, and repetitive forms of physical activity to maintain or improve fitness in a specific dimension.³⁵ In the same vein, we propose that passive movement can be defined as any externally driven limb or body movement that does not require voluntary muscle contraction, typically performed to support individuals with physical disabilities or limited mobility, whereas passive exercise refers to a planned, structured, and repetitive form of passive movement designed to promote specific physical, cognitive, or mental health outcomes. There exist “hybrid” active-passive modalities (e.g., partially assisted cycling) which have been used in the context of rehabilitation and to support persons with Parkinson’s disease.^37,38 We classify these modalities as primarily “active” given that the participant’s volitional movements are supplemented by some external force.