Postural Control in Diabetic Peripheral Neuropathy: A Narrative Review

1. Postgraduate Student, Department of Neuro Physiotherapy, College of Physiotherapy, Sumandeep Vidyapeeth an Institution Deemed to be University, Vadodara, Gujarat, India. 2. Assistant Professor, Department of Neuro Physiotherapy, College of Physiotherapy, Sumandeep Vidyapeeth an Institution Deemed to be University, Vadodara, Gujarat, India. 3. Professor, Department of Neuro Physiotherapy, College of Physiotherapy, Sumandeep Vidyapeeth an institution Deemed to be University, Vadodara, Gujarat, India.

Abstract

Diabetes mellitus is a metabolic disease of chronic hyperglycaemia which leads to neurological complications such as Diabetic Peripheral Neuropathy (DPN). When compared to healthy persons, those with DPN are more likely to fall, especially in geriatric population. Present review aims to provide an insight to the pathophysiology, outcome measures, and physiotherapy treatment of impaired postural control in DPN. Searches for relevant articles were conducted using Google Scholar, PubMed, Ovid, Springerlink, Science Direct (SD), Seniorcare Ageing Growth Engine (SAGE), Elton B. Stephens Company (EBSCO) Discovery Service and Web of Science. Keywords used were diabetes, DPN, diabetic foot, postural control, balance, postural sway, physiotherapy intervention. Irrespective of their year of publication, studies and reports published in English, that provide data of postural control in individuals with DPN and its physiotherapy management were included in the study. The included publications were reviewed and a narrative review was formulated. A total of 35 studies were included in this review. All studies suggest that there is postural instability in people with DPN which increases with age and duration of diabetes. Multidirectional postural sway was observed in most of the studies with medio-lateral instability encountered in more cases. Significant improvement in timed up and go test, single leg stance test, Berg balance scale, and other outcome measures post physiotherapy intervention were reported. Literature suggests that multidirectional postural instability is present in DPN patients. Physiotherapy, offloading devices and diabetic foot care education improve postural stability in individuals with DPN.

Balance, Diabetic foot, Diabetes mellitus, Neurological complications, Postural sway, Physiotherapy

Diabetes mellitus is a metabolic disease where chronic hyperglycaemia occurs due to abnormality in insulin secretion, insulin action, or both (1). The number of people with diabetes in India increased from 26.0 million in 1990 to 65.0 million in 2016 (2). Diabetes mellitus leads to macrovascular as well as microvascular complications (3). Because of hyperglycaemia, there is a defect in both nerve function and structure which leads to neurological complications such as diabetic neuropathy (4).

Postural control means controlling the body’s position in upright posture for the purpose of stability and orientation (5),(6). The ability to maintain the Centre Of Mass (COM) in relationship to base of support is termed as postural stability. Postural sway is the displacement of centre of gravity within the base of support and with a larger sway path there is greater postural unsteadiness. Postural control for stability and vertical orientation requires a complex interaction of musculoskeletal and neural system (6). In diabetic neuropathy, there is lack of accurate proprioception, visual and vestibular problems and impaired motor function which leads to postural instability (5). Impaired postural control in diabetic individuals causes increase postural sway which leads to balance problems and high risk of fall in older DPN patients (3),(7).

When compared to healthy persons, those with DPN are more likely to fall, especially in geriatric population (8). As a result, it is critical to understand the factors that influence falls in DPN patients, such as postural control deficit and available physiotherapy measures to improve postural control in DPN. The present review aimed to study majority of published studies to date on the effects, features, and physiotherapy treatment of abnormalities in postural control in DPN.

LITERATURE SEARCH

The literature was searched using various search engines like Google Scholar, PubMed, Ovid, Springerlink, Science Direct (SD), SAGE, EBSCO Discovery Service and Web of Science databases, etc., Hand search of articles were also done in the University library. In effort to compile vital information published till date, the articles published in English language and irrespective of the year of publication were screened for inclusion criteria.

Inclusion criteria: All those studies (systematic review, meta-analysis, randomised control trials, cohort studies, case control studies, narrative reviews and case series) and reports that provided data on the postural control in diabetic neuropathy and its physiotherapy treatment were included for review.

Exclusion criteria: The animal studies and studies done on diabetic patients without diabetic neuropathy were excluded.

The study strategy identified a total of 233 studies, following the removal of duplicates and the screening of titles and abstracts, a total of 141 potentially relevant studies were excluded. Remaining 92 studies were analysed for the inclusion criteria to determine if they should be considered as a part of this study or not, which further excluded 57 articles, and at last 35 studies remained. From these 35 articles, a narrative review on postural control in DPN patients was formulated (Table/Fig 1). The included articles were critically appraised for appropriateness of the study design for the research question, key methodological features, statistical methods used and their subsequent interpretation, potential conflicts of interest and the relevance of the research to present study aim.

DIABETIC NEUROPATATHY

DPN include varying disorders that involve a wide range of abnormalities affecting both peripheral and autonomic nervous systems, leading to significant rise in morbidity and mortality. These neuropathies can be focal or diffuse, proximal or distal, and could also affect somatic and autonomic nerves (Table/Fig 2) (9),(10),(11),(12).

Clinical Presentation of Diabetic Peripheral Neuropathy (DPN)

(Table/Fig 2) depicts the comparative analysis of various clinical signs and symptoms and pathophysiologies associated with them (9),(10),(11),(12).

DPN is progressive, degenerative and is classified into three main types:

• Sensory neuropathy
• Motor neuropathy
• Autonomic neuropathy

The classical feature observed in DPN is of “gloves and stockings” distribution. The symptoms frequently worsen throughout the night and create sleep problems, lowering one’s quality of life. During the initial phase of the disease patients usually complain of allodynia which is characterised as alteration in perception of pain and temperature, tingling, and burning sensation. This occurs because of active degenerative of nerve fibres or due to compromised regeneration process (10),(11). As the condition progresses, symptoms also increase and gradually there is complete loss of sensation, called as anaesthesia along with progression of symptoms from distal to proximal portion.


Vibration sensation is typically the first sensation that is found to be lost in DPN (10). The presence of neuropathy is associated with increased body sway and foot ulceration. Foot instability increases in foot ulcer patients due to defects in proprioception. Thus, diabetic patients with a history of foot ulceration have significantly increased body sway with increase in vibration perception threshold (13). Pain or paraesthesia is also a clinical feature seen in patients with DPN which occurs because of active degeneration of nerve fibres or due to compromised regeneration process (11). As the disease progresses, there is complete loss of pain sensation which increases the risk of trauma and causes serious ulceration (12).


If no strict action is taken to control blood glucose level and the sensory symptoms being ignored, it would further damage motor and autonomic nerve fibres and will lead to motor and autonomic dysfunctions. Motor neuropathy causes a variety of foot abnormalities (deformities) because of intrinsic muscle weakness. Foot abnormalities can be as simple as hammer toe deformity or as severe as Charcot Arthropathy, which affects the anatomic architecture of the foot (10). Hence, both sensory and motor impairments in DPN will result into unequal foot loading resulting to abnormal gait and history of frequent falling with higher chances of foot ulceration (12),(13) and in later stages limb amputation is done (10).

Autonomic neuropathy will lead to alteration in the integrity of skin because of disturbance in cutaneous blood flow, loss of normal perspiration and activity of oil glands (10). This results in dry and fragile skin vulnerable to injury. Clinically, diabetic foot ulcers are presented in circular shape surrounded by hyperkeratotic borders which are usually developed at the area of constant high pressure (12).

Beside this, there are few recent studies that have stated that the central nervous system is also involved. Presynaptic inhibition either inhibitory or excitatory spinal reflex, helps in maintaining balance and postural stability. A study done by Chun J and Hong J aimed to find out the relationship between presynaptic inhibition and DPN in ability to control postural stability (14). He found out that people with DPN had reduced presynaptic inhibition and also had decreased balance leading to increased postural sway. The possible reason could be that presynaptic inhibition is responsible for fine motor control and so, people with less presynaptic inhibition tends to have less fine motor control followed by instability (14).

Postural Control in Diabetic Peripheral Neuropathy (DPN)

Posture is a complex task which demands the gathering and integration of sensory (afferent) information to coordinate effectively with the neuromusculoskeletal system in order to maintain balance. The peripheral sensory systems involved are the vestibular apparatus, the visual system, and the kinesthetic and proprioceptive receptors which are widely distributed throughout the body (15). Apart from this, body alignment, muscle tone and postural tone contributes in maintaining postural stability. They help in maintaining the effect of gravitational force acting upon the body and help in preventing the body from collapsing due to the pull of gravity (6). Afferent fibres of lower limbs play an important function in reflex control of the body during a quiet upright stance (16).

Alteration in any of these systems leads to increased body sway leading to postural control disturbances. It could be because of failure of the lower extremities and postural muscles to generate an adequate amount of activity. Strength of lower extremity muscles decreases in neuropathy especially of ankle flexor and extensor muscles of DPN patients (17). This reduction in muscle strength is found to be linked with higher glucose concentrations (18),(19). In addition, there is compromised reflex activity of lower extremity muscles (20). Along with reduction in muscle strength and deterioration in reflex response, the spinal sensation of muscles i.e., position, velocity, and force sensation components are also compromised. Thus, DPN degrades the motor and sensory function which causes poor balance in DPN patients (21),(22).

Dixit S et al., and Boucher P et al., found that individuals with neuropathy had significantly raised sway speed, velocity moment and mediolateral and anteroposterior displacements under four conditions- eye open, eye close, eye open on foam and eye close on foam (23),(24). Standing with eyes closed worsens their postural stability in individuals with diabetic neuropathy. Also, with increase in duration of diabetes, postural stability was more affected. The postural stability in DPN individuals is affected even in quiet stance and could increase the risk of fall when on foam or deformable surface (7),(23),(24).

Mustapa A et al., performed a systematic review which revealed, DPN contributes to abnormal postural control by causing impairments in proprioceptive and tactile sensation (somatosensory input) and reduction in reaction time and muscle strength (motor output) (7). Reduction in ankle strategy was present and if combined with visual defect was resulting in greater postural sway in DPN (25). The review also reported lower equilibrium score, lower balance score in berg balance scale, larger trace surface area, with faster mean velocity of body sway in eye open and closes condition in patients with DPN (7).

Vaz MM et al., and Melo TA et al., reported Type 2 Diabetic Mellitus (Type 2 DM) patients took more time to complete Five-Times-Sit-to-Stand Test (FTSST compared to non diabetic people, suggesting that those with Type 2 DM have higher risk of falls during dynamic situations in which integration of several body components, such as sensory system, motor coordination, mobility and muscle strength are required (26),(27).

In order to maintain Antero-Posterior (AP) stability, the ankle strategy is normally used, which is often affected in individuals with DPN (25). On the other hand, the hip joints have a greater impact on Medio-Lateral (ML) stability, with alternating action of the abductor and adductor muscles (23),(28). Because of reduction in ankle strategy, a compensatory greater use of hip strategy in seen in DPN [23,29]. Lim KB et al., reported that while testing static and dynamic balance abilities with Modified Clinical Test Sensory Interaction on Balance (mCTSIB), individuals with DPN showed more balance instability than both diabetic control and non diabetic control patients (22). Fortaleza AC et al., found that DPN group had worse ML instability during semi-tandem stand (28). ML stability is more affected even with vision in DPN patients (28),(30),(31). Dixit S et al., reported multidirectional postural instability in DPN individuals. Hence, management should not only direct towards one strategy (23).

During gait activities like ground level walking, stair ascent and descent; balance is greatly impaired in patients with DPN (32). This is because while walking an individual transfers his/her weight from one limb to another causing brief periods of large separation between centre of mass and the centre of pressure (33). To maintain balance during these period, high levels of muscular strength is required which is compromised in DPN patients [33,34]. Thus, they have higher risk of falling during gait activities than during quiet standing. A study done by Brown SJ et al., concluded that balance impairment with DPN is predominantly in the ML plane and was greatest during stair descent (33). Also, shortening step length is a common strategy used among those who are at higher risk of falling (35). This maintains a closer control of the centre of mass above the centre of pressure, thereby reducing muscular demands and the risk of falling (33). Individuals with DPN tend to have temporal-spatial parameters of the gait affected, and have greater gait variability. Impaired perturbation response also potentially increases the risk of falling (7).

Ghanavati T et al., reported that elderly individuals with DPN had a considerably lower total score of Berg Balance Scale (p-value <0.001) in comparison to healthy age matched individuals (36). DPN patients had significantly lower scores in tasks like standing on one leg, standing unsupported with one foot in front, reaching forward without stretched arm while standing, standing independently in narrow Base of Support (BOS), stand to sit, sit to stand, transfer activities, turning, standing independently with eyes close and stepping on stool while standing unsupported. (Table/Fig 3) depicts the comparative analysis of postural control impairment and alteration in gait performance in DPN patients and various inferences drawn from them. Thus, elderly with DPN are more unstable while performing their activities of daily living (Table/Fig 3) (7),(14),(15),(16),(21),(22),(23),(24),(26),(28),(29),(31),(33),(34),(36).

Assessment of postural control in diabetic patients: There are several outcomes measures ranging from advance technology to clinical tests and functional scales by which we can assess the postural stability in diabetic neuropathy patients. Static, dynamic and functional balance tests like One Leg Stance (OLS), Functional Reach (FR) test and TUG are been developed and have shown to have good reliability, validity and responsiveness in older population and people with balance impairment (37),(38),(39),(40). Dominguez-Muñoz FJ et al., reported the reliability of TUG in diabetic neuropathy patients (41). Intraclass Correlation Coefficient (ICC) was higher than 0.90 (excellent) in individuals having moderate neuropathy and individuals with normal foot vibration perception. Whereas, it was found just good in individuals with severe neuropathy with ICC as 0.70-0.90. He also found that time required to complete TUG was more in individuals with severe DPN (41).

The Wii Balance Board (WBB) and Pedalo®-Sensomove balance device have also demonstrated to be a highly valid and reliable method for assessing the COP range and COP displacement (sway) during different balance tests in older adults with Type 2 DM and in individuals with DPN (40),(42).

A systematic literature review carried by Dixon CJ et al., found that commonly used clinical balance measures for people with Type 2 DM and DPN do not assess all systems of balance, and most of them have not yet been validated in a Type 2 DM and DPN population (43). Therefore in future, studies are required to establish reliability and validity of these tests in patients with Type 2 DM and DPN (Table/Fig 4) (38),(40),(41),(42),(43).

Physiotherapy Management

The sensory-motor deficits in patients with DPN leads to balance problems, risk of falling and further alteration in motor programming. Therefore, it is important to focus on sensorimotor training (balance training). Sensorimotor training helps in adequate recruitment of various muscles responsible for maintaining stability of the body (44).

Ahmad I et al., found that sensorimotor and gait training was an effective treatment protocol in order to achieve improvement in proprioception and nerve function (44). Exercise was conducted on alternate days, thrice a week for 8 weeks. Each session consisted of 10 minutes of warm-up (treadmill/cycle ergometer), followed by 50-60 min of exercise (wall slides, bridging exercises, prone plank, sit to stand, wobble board exercise, one leg stand, heel to toe raise, tandem stance, walking on line, tandem walk, high march tandem walk and high arch tandem backward walk) and ended with cool down (deep breathing exercise, abdominal breathing and mild stretching) for 5-10 minutes. Progression was done by incorporating unstable surfaces. Positive effect was observed in proprioception in all directions, nerve conduction velocity and in electromyographic activities recruiting tibialis anterior, medial gastrocnemius and multifidus. Also, sensorimotor and gait training was found feasible and easy to be used in the clinical set-up as well as home exercise, protocol in patients with DPN due to lesser risk (44). It is believed that with balance exercise, there is stimulation of mechanoreceptors present in muscle spindle, Golgi tendon organ and joint capsule leading to improvement inputs of proprioception from foot, ankle and trunk. Repetitive ankle and foot movement while performing exercise also improves proprioception (44),(45).

In an Randomised Clinical Trial (RCT) by Ahmed I et al., effect of eight weeks of sensorimotor (balance) training and diabetes and foot care education on postural control was evaluated using Functional Reach Test (FRT), TUG, OLS and Pedalo®- Sensomove balance Test Pro (46). There was significant improvement found in FRT, TUG, COP range, OLS and proprioception. The improvement was greater in the middle-age group compared to older adults with DPN possibly because of aging and longer duration of DPN (46).

In elderly with DPN, resisted training of lower limb along with ankle strategy training helps in enhancing muscle strength of foot and ankle improves the ability to walk and balance (45),(46),(47),(48). Allet L et al., conducted an RCT on diabetic patients with minimal neuropathy (47). Experimental group received exercise sessions twice a week for 60 minutes for 12 weeks. Starting with warm up for 5 minutes followed by circuit training for 40 minutes which involved gait and balance exercise (stance on heel/toe, tandem stance, OLS, functional strength training, endurance exercise, walking up and down a slope, sit to stand, mini hops, stair climbing and interactive games like obstacle race and badminton). Tasks were performed twice for one minute and then challenges were added by changing to unstable surfaces, increasing step height. Postintervention, there was improvement in patients’ habitual walking speed by 0.149 m/s (0.54 km/h; p<0.001) compared to control group. Also, clinically significant improvement in static and dynamic balance was noted (p<0.0026) (40). Increased strength of hip and ankle musculature and its mobility could be possible reason for this improvement (45),(47). Similar findings were reported by Pan X and Bai JJ, (48) who reported that weight training for 12 weeks could significantly improve the lower limbs strength and thereby walking ability in patients with DPN (45),(48).

Elderly having DPN often suffer with vestibular dysfunction. The sensitivity levels of the vestibular system are attributable to high blood glucose and insulin level, which leads to impaired balance by large anterior translation of the body (7),(48). It also leads to disturbance in integrating information to the brain leading to difficulty in maintaining balance resulting in increased risk of falling. Thus, it is important to train vestibular functions in the form of rotational movement, posture reactive movement etc. It aids in the rapid processing of sensory signals, as well as making the correct judgment motion response through sensory reorganisation (48).

Najafi B et al., used plantar electrical stimulation for improving postural balance and plantar sensation in DPN patients (49). Transcutaneous Electrical Nerve Stimulation (TENS) (SENSUS®) with duration of 60 minutes with the placement of electrodes in hind and midfoot area was applied daily for six weeks. The post-treatment results were significant and there was improvement in plantar sensation by 27% in the intervention group. These findings were similar to previous studies which stated that following electrical stimulation treatment, there is reduction in vibration perception threshold which further leads to increase chances of monofilament detection in people with DPN (49).

Tai Chi exercise and Thai foot massage are also effective in glucose control, neuropathy score, balance control, improving protective sensation and in improving quality of life in patients with DPN (47). A systematic review done by Gu Y and Dennis SM included two studies regarding Tai-Chi as an intervention (45). After Tai-Chi intervention there was significant improvement in single leg stance (baseline 32.5±3.3 seconds to postintervention 34.6±2.4 seconds (6.46%), p=0.004) and reduction in time required for performing 8-foot up and go test (baseline 9.2±3.3 seconds to postintervention 8.3±2.0 seconds, p=0.02). This led to improvement in gait measures like stride length and time spent in single leg support aiding their participation in social life (45).

Balance training can also be given with Biodex Balance System (BBS). BBS is considered to be an effective tool for training balance and postural stability. Eftekhar-Sadat B et al., measured diabetic and peripheral neuropathy subject’s ability to maintain balance performing functional tasks using BBS (30). For balance training, subjects were asked to touch target points using an on-screen cursor with subjects legs placed on the platform. Both static and dynamic balances were assessed by using usual tasks such as reach, standing position and transferences. There was significant reduction observed in TUG, fall risk index with higher changes in berg balance scale. Thus, its result proved that balance training was effective in gaining postural stability and balance in elderly patients with DN (30).

Exercising in people with diabetes is limited in some older people with DPN because they have high risk for falls. So, an alternative intervention is required which effectively addresses the loss of plantar sensation and helps in improving balance, reduces fear of fall and increases participation. Conventional training is not always appropriate for all DPN patients as it decreases the accuracy of exercise performance and has higher risk of excessive plantar loading which could lead to foot ulcers (50). Grewal G et al., used sensor-based interactive balance training including visual joint movement feedback for enhancing postural stability in patients in DPN (51). There was significant reduction in centre of mass sway area for intervention group by 53.81% with eyes open. Also, their quality of life and performance of daily physical activities showed improvement (51). Rao N and Aruin AS used auxiliary sensory clues as a balance prosthesis to improve balance and postural stability in individuals with sensory neuropathy (52). Sensory clues were provided to the calf with the help of a device similar to Ankle Foot Orthosis (AFO) with no additional stabilisation of the ankle joint. However, no significant improvement in static balance was found (52).

While training elderly population, it is important to start with lower intensity resistance training using major muscle groups. The progression is done gradually by increasing the intensity (53). A minimum duration of 40 minutes is necessary to have the best effect with strict adherence to exercise protocol (54). Groups or music mediated sports training and campaign training can help in motivating and encouraging elderly population with DPN to adhere to their exercises (48).

Foot care education, techniques to reduce pressure over diabetic foot and glycaemic control are also important part of management. Offloading plays an important component of treatment in order to prevent or heal foot ulcers (52),(55). Offloading devices of numerous types (soft and shock absorbing materials, custom moulding, forefoot offloading devices and rocker-bottom shoes, total contact casts, walkers and braces) have shown significant improvement (55),(56),(57). When Sorbothane and calcaneal heel pad were used together as an insole material, the shock attenuation was found to be only 18%. However, standing on soft materials further disturbs postural stability (58). So, while choosing insole material it is important to keep in mind both the offloading effect and its effect on postural stability. High resilience material tends to give more bouncy effects whereas low resilience material has more dampening effects. Thus, low resilience materials offer more stability. Increased plantar contact area leads to improved cutaneous feedback from the plantar surface thus, enhancing inputs for postural control (57). Wear and tear of shoes could also affect postural stability and could lead to fall (59). A custom-molded insole fitted inside a fixable shoe gives 20% of offloading in the forefoot but a cast shoe with molded rigid sole gives 48% offloading (Table/Fig 5) (30),(44),(45),(46),(47),(48),(49),(51),(52),(55),(57),(60).

Conclusion

This review highlights the evidence that reduced sensation including proprioception and muscle strength of distal lower limb lead to multidirectional postural instability in patients with DPN. Early integration of sensory-motor training, balance training and gait training are beneficial in improving postural control in individuals with DPN. In elderly with DPN, vestibular rehabilitation, resistance training of lower limb muscles and ankle strategies training are effective in improving postural control. Foot care education and offloading devices with low resilience materials, helps in improving postural control and reducing risk of foot injury in individuals with DPN.

DOI and Others

DOI: 10.7860/JCDR/2022/52191.16273

Date of Submission: Sep 02, 2021
Date of Peer Review: Nov 11, 2021
Date of Acceptance: Feb 16, 2022
Date of Publishing: Apr 01, 2022

AUTHOR DECLARATION:
• Financial or Other Competing Interests: None
• Was Ethics Committee Approval obtained for this study? NA
• Was informed consent obtained from the subjects involved in the study? NA
• For any images presented appropriate consent has been obtained from the subjects. NA

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