Inconsistent findings from laboratory studies have made it difficult to determine which gait alterations are specific to diabetic peripheral neuropathy and which also affect diabetic patients without neuropathy. Body-worn sensor technology may help clarify the distinctions.
By Tahir Khan, DPM, and Ron Guberman, DPM, DABPS
According to the American Diabetes Association more than 25 million Americans have diabetes while another 79 million are prediabetic1,2 and estimates suggest that one in four US adults aged 65 or older has diabetes.1 Many serious medical conditions have an increased prevalence among patients with diabetes. The risk of heart disease and stroke is two to four times higher in diabetic patients than in the general population; in addition, up to 70% of diabetic patients have hypertension, while another 28% have diabetic retinopathy.1 Diabetes is also the leading cause of kidney disease, including end-stage renal disease and kidney transplants, and 60% to 70% of patients with diabetes have diabetic peripheral neuropathy.1
Diabetes is the leading cause of nontraumatic lower extremity amputations in the US, with more than 65,000 nontraumatic lower extremity amputations performed on diabetic patients in 2006.1,2 US employers spend more than $130 billion annually in direct and indirect costs related to diabetes.3 Diabetes is also considered an independent risk factor for falls among the elderly. In a prospective study of 139 elderly patients, Maurer et al concluded that diabetes, gait, and balance are independent predictors for a heightened risk of falling.4
A better understanding of gait alterations in diabetic patients will help clinicians educate patients and prevent many lower extremity complications associated with diabetes and diabetic peripheral neuropathy. These complications include falls and injuries resulting from altered gait patterns and abnormal lower extremity biomechanics.
Diabetes and neuropathy
Diabetes mellitus is a metabolic condition primarily defined by hyperglycemia. In diabetic patients, either the body does not produce enough insulin or the cells do not respond properly to the insulin produced by the body. Diabetic patients commonly present with the classic symptoms of polyuria, polydipsia, and polyphagia. There are three main types of diabetes. Type 1, also called insulin-dependent diabetes mellitus, results from the loss of insulin-producing beta cells in the pancreas, leading to insulin deficiency. Type 2 is caused by insulin resistance of the receptor cells. The third type, gestational diabetes, involves pregnant women with no past medical history of diabetes developing hyperglycemia during pregnancy.5-8
Diabetic peripheral neuropathy is one of the most common and debilitating complications of diabetes and accounts for significant morbidity and mortality by predisposing the foot to neuropathic ulceration that can lead to lower extremity amputation.9 Diabetic peripheral neuropathy affects all peripheral nerves, including pain fibers, motor neurons, and the autonomic nervous system. The most common symptoms of diabetic peripheral neuropathy include numbness, tingling, pain, and allodynia.5-8 A predominant feature of diabetic peripheral neuropathy is sensory loss, which can lead to foot ulcerations and amputations.
Several pathways are thought to be involved in the development of diabetic peripheral neuropathy.
1. Microvascular disease. Microvascular dysfunction occurs early in diabetes and as the disease progresses; neuronal dysfunction correlates closely with vascular dysfunction leading to neuronal ischemia, a well-established characteristic of diabetic neuropathy.5-8
2. Advanced glycated end products. Elevated intracellular levels of glucose cause alterations in the structure and function of many different proteins. Several of these proteins are involved in causing diabetic peripheral neuropathy and long-term complications of diabetes.5-8
3. The polyol pathway, also called the sorbitol/aldose reductase pathway. A polyol is an alcohol containing multiple hydroxyl groups. In the polyol pathway glucose is first converted to sorbitol and then to fructose. The polyol pathway results in microvascular damage to the nervous tissue, causing diabetic peripheral neuropathy.10
Different nerves are affected in different ways. Sensorimotor polyneuropathy involves decreased sensation and loss of reflexes. Decreased sensation and loss of reflexes occurs first in the toes and then may extend proximally. This occurs because long nerve fibers are affected at a much higher rate than short nerve fibers; nerve conduction slows in proportion to the nerve’s length. Patients most commonly present with numbness, burning, tingling sensations in the feet, and loss of proprioception. Numbness and loss of sensation can lead to injuries from inadvertently stepping on foreign objects or to ulcers, infections, and amputations caused by ill-fitting shoes.5-8
Autonomic neuropathy affects the nerve fibers of heart, lungs, blood vessels, gastrointestinal system, and genitourinary system. In a study published in Diabetes Care researchers concluded that patients with painful diabetic peripheral neuropathy had a much greater risk of autonomic dysfunction.11 The most common autonomic dysfunction involves orthostatic hypotension. Other manifestations include gastroperisis, leading to bloating and diarrhea. Genitourinary manifestation may involve urinary frequency, urgency, incontinence, and retention. Urinary retention may lead to urinary tract infections.5-8
Diabetic peripheral neuropathy is most commonly diagnosed through a thorough physical examination that may include a vibration perception examination involving a 128-Hz tuning fork, a 5.07/10-g Semmes-Weinstein monofilament, or a calibrated vibration perception threshold (VPT) meter.9
New avenues in gait analysis
Gait has historically been analyzed in specialized gait labs. A gait laboratory with a video camera system and a walkway with implanted sensors12,13 is an excellent way of measuring gait and is considered the gold standard, but has several drawbacks. It is very expensive and requires a dedicated laboratory. A tremendous amount of time is required for equipment setup and data analysis. Gait analysis inside a gait lab also requires study participants to walk in a predetermined space that usually allows for no more than a few gait cycles and does not reflect the real-life natural environment in which humans function.14 Our daily activities require us to walk in challenging environments and on varied surfaces. Studies have shown that irregular and challenging environments influence gait parameters and may increase the risk of falls, especially in elderly and compromised patients.15,16
To avoid these limitations, and thanks to advances in technology, body-worn sensor-based systems are increasingly being used to measure different aspects of gait. These include spatiotemporal parameters,14,17 joint and segment angles,12,17-18 measures of daily physical activity,19-23 and risk of falling as well as fear of falling.24 One of the main advantages of body-worn sensor technology compared with laboratory based systems is that the sensors can be used outside of the gait laboratory.25,26 They are also lightweight and can be used for long periods.25,26 Thus, body-worn sensors seem ideal for gait analysis in many different environments, both inside and outside of the gait laboratory.
Review of literature
Several studies have evaluated gait alterations in diabetic patients. Petrofsky et al27 evaluated gait characteristics of 15 patients with type 2 diabetes and compared them with 16 healthy controls. Diabetic patients with peripheral neuropathy were excluded from this study. The authors found that patients with diabetes walked significantly slower than healthy controls and had a wider stance.
In a study published in Diabetes Care in 1997, Katoulis et al28 evaluated the effects of diabetic peripheral neuropathy in 20 neuropathic diabetic patients without a history of foot ulceration and compared their results with 20 healthy controls, 20 non-neuropathic diabetic controls, and 20 neuropathic diabetic patients with a history of foot ulceration. The study found no statistically significant gait differences between controls and non-neuropathic diabetic patients. The diabetic patients with peripheral neuropathy demonstrated alterations in some gait parameters during walking compared with control groups, and walking speed was significantly slower in diabetic neuropathic subjects with a history of foot ulceration than in other groups.
These two studies seem to contradict each other, with Petrofsky et al27 noting differences in the gait pattern of non-neuropathic diabetic patients while Katoulis et al28 did not. Both of these studies were performed in gait laboratories, a method that, as previously mentioned, has several drawbacks.
Two studies using body-worn sensors to evaluate gait in diabetic patients are worth mentioning. In the first study investigators used using body-worn sensors in a natural environment outside of the gait lab to evaluate walking behavior of elderly diabetic patients on irregular surfaces. In the 2008 study, researchers evaluated the gait pattern of 16 patients with type 2 diabetes (with and without neuropathy) twice in eight days. Patients were included in the study if they had type 2 diabetes (with or without neuropathy) and were excluded if they had a concomitant foot ulcer; orthopedic, surgical, or neurological condition influencing gait; or nondiabetic neuropathy.15
Participants were asked to walk on three different surfaces: two 50-m tarred pathways, two 50-m grass pathways, and two 20-m cobblestone pathways. The order of the surfaces patients walked on was randomized and the identical procedure was repeated after eight days. This study indicated that body-worn sensors provided a reliable assessment of gait parameters in an outdoor setting and on different surfaces. The authors concluded the irregular surfaces influenced gait parameters such as speed, cadence, gait cycle time, and the maximal sagittal shin angle velocity. The patients walked slower on cobblestones than on grass and slower on grass than on the tarred pathway. The authors further concluded that influencing gait speed in an elderly diabetic population at high risk of falling is of high clinical value.15
Another study from the same research group in 2009 evaluated gait parameter changes on irregular surfaces using body-worn sensors in 30 patients with type 2 diabetes (15 with neuropathy and 15 without neuropathy) and compared results with 15 healthy controls. The participants in this study were asked to walk on the same three surfaces as in the previous study.16
This study noted significant differences in gait parameters between diabetic patients without peripheral neuropathy and healthy controls, including speed, cadence, and gait cycle time. When comparing diabetic patients with peripheral neuropathy with healthy controls, all parameters of gait (velocity, cadence, stance, double support time, gait cycle time, and stride) were significantly different with the exception of shank and knee angle. No differences in gait parameters were observed between diabetic patients with peripheral neuropathy and those without.
In general, all gait parameters were significantly altered by the surface, with gait alterations observed with greater sensitivity on irregular surfaces. The 2009 study indicated that gait parameters deteriorated with peripheral neuropathy and that changes in gait were more pronounced among diabetic patients with neuropathy, followed by non-neuropathic diabetic patients, followed by the healthy control group. This study concluded that some of the diabetic patients’ gait parameters were altered (there was a decrease in speed and cadence followed by shortening of stride length) even before neuropathy was clinically detected and that clinicians should be aware that diabetic individuals’ gait capacity decreases and fall risk increases at an early stage of the disease. The differences in the gait pattern of diabetic patients without peripheral neuropathy noted in this study are in line with the study by Petrofsky et al, and may suggest that gait abnormalities occur across the spectrum of diabetes but increase with disease severity.16 Possible causes of these gait alterations proposed by the authors include small fiber damage, impaired sight or simple retinopathy, vestibular disorders, or a combination of several of these factors. This study further concluded that decreased gait velocity in diabetic patients without peripheral neuropathy is of high clinical relevance as it could influence their activities of daily living.16
In a recent study done by our group at the Center for Lower Extremity Ambulatory Research at Wyckoff Heights Medical Center in Brooklyn, NY, we compared gait parameters of 12 diabetic peripheral neuropathy patients with eight healthy controls. All participants were asked to walk barefoot and wearing their regular shoes at their habitual speed over a short (7 m) and long (20 m) distance. We measured diabetic peripheral neuropathy using the vibratory perception threshold meter.
Our results indicate that patients with diabetic peripheral neuropathy had more gait unsteadiness than controls and required longer periods of double support time, especially when walking barefoot over the long walking distance. Our results also indicated that gait unsteadiness was highly correlated to worsening vibratory perception in diabetic peripheral neuropathy patients, meaning the worse the peripheral neuropathy, the higher the gait unsteadiness.
Interestingly, when patients with diabetic peripheral neuropathy were asked to walk wearing shoes, their gait unsteadiness improved significantly and the number of steps required to achieve a steady state of walking decreased, suggesting these patients benefit from wearing shoes when walking.29
Diabetes has been described as an epidemic in the US, with the Centers for Disease Control and Prevention (CDC) indicating that 1.9 million people were newly diagnosed with the disease in 2010.1 If current trends continue, the CDC estimates one in three Americans will develop diabetes sometime in their lifetime.1 As the prevalence of diabetes and diabetic peripheral neuropathy continues to increase, and as we continue to spend billions of dollars treating diabetes and its associated complications, healthcare practitioners and researchers need to be more vigilant and proactive in using advanced technologies to understand and manage these conditions.
Knowledge of gait alterations in diabetic patients is of high clinical value as it would help clinicians educate patients and prevent many lower extremity complications associated with diabetes and diabetic peripheral neuropathy. These complications include falls and injuries resulting from altered gait patterns and abnormal lower extremity biomechanics.
In a randomized controlled trial published in Diabetologia, 35 diabetic patients went through gait and balance exercises for 12 weeks. After 12 weeks of exercises diabetic patients improved their habitual speed, balance, and mobility, their degree of concern about falls, hip and ankle plantar flexor strength, and hip flexion mobility. The authors of this study concluded that specific training interventions could improve gait speed, balance, muscle strength, and joint mobility in patients with diabetes.30 Future studies should focus on abnormal biomechanics that may lead to injuries such as sprains and strains, foot ulcerations, and Charcot neuroarthropathy. Armed with this knowledge, healthcare practitioners will be better equipped to prevent many lower extremity complications in patients with diabetes and diabetic neuropathy.
Tahir Khan, DPM, is a first year resident and Ron Guberman, DPM, DABPS, is director of Podiatric Medical Education and co-chief of the Podiatry Division in the Department of Surgery at Wyckoff Heights Medical Center in Brooklyn, NY.
Disclosures: The authors report no conflicts of interest or financial support received.
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