Risk assessment of the diabetic foot and wound

Abstract

Diabetic foot ulcers are among the most common severe complications of diabetes, affecting up to 68 per 1000 persons with diabetes per year in the United States. Over half of these patients develop an infection and 20% require some form of amputation during the course of their malady. The key risk factors of diabetic foot ulceration include neuropathy, deformity and repetitive stress (trauma). The key factors associated with non healing of diabetic foot wounds (and therefore amputation) include wound depth, presence of infection and presence of ischaemia. This manuscript will discuss these key risk factors and briefly outline steps for simple, evidence‐based assessment of risk in this population.

Introduction

Complications of the diabetic foot are the most common cause of non traumatic lower extremity amputations in the world. Individuals with diabetes have up to 46‐fold greater risk of high‐level lower extremity amputation than those without diabetes (1, 2). The single most common factor leading to amputation is the neuropathic diabetic foot ulcer. The diabetic foot ulcer is amongst the most common of diabetic foot complications, affecting some 68 per 1000 persons with diabetes per year in the United States (US). Over one half of these patients develop an infection (3, 4). While the majority of these infections may be treated on an outpatient basis, the infected foot ulcer is the most common reason for hospitalisation among patients with diabetes, accounting for approximately one quarter of all diabetes‐related admissions in the US and United Kingdom 5, 6, 7).

Unfortunately, the majority of patients admitted to the hospital for diabetic foot complications receive a less than adequate lower extremity evaluation. Edelson and coworkers (8) reported that only 14% of patients admitted to the hospital with a diabetic foot complication received appropriate and adequate lower extremity evaluations. It has been estimated that appropriate knowledge of risk factors and application of evidence‐based multidisciplinary treatments could reduce 85% of diabetic foot and leg amputations (9, 10). Prevention is becoming increasingly important to overburdened health care systems in industrialised nations. This is exemplified by the fact that only 2% of patients receiving an amputation are admitted from an intermediate or long‐term care facility and 25% are discharged to one following the amputation (11).

Regular inspection is one of the most effective mechanisms to prevent diabetic foot complications. Even with an increase in diabetic foot awareness, there still exists a tremendous deficiency in foot evaluations. Persons with diabetes often do not have their feet evaluated, even on the most cursory level, during a regular office visit by their primary care physician, with only 10–19% of patients with an established diagnosis of diabetes had their feet inspected even after having their shoes and stocking removed by the nursing staff (12, 13). The majority of the signs and symptoms associated with ulceration and amputation can be identified by a few focused questions, foot inspection and simple examination techniques. This manuscript will review the risk factors most commonly associated with lower limb ulceration in the diabetic population and will subsequently outline a treatment‐based classification system for risk stratification and subsequent treatment.

What are the risk factors of diabetic foot ulceration?

The most common risk factors for ulceration include peripheral neuropathy, history of ulceration and structural deformity (14, 15). While myriad other factors exist, such as peripheral arterial disease, poor metabolic control, blindness and poor social support systems 16, 17, 18), these are generally secondary factors that do not in and of themselves lead directly to diabetic foot ulceration.

Peripheral neuropathy

Peripheral sensory neuropathy is one of the most significant risk factors for both foot ulceration and amputation in this population (6). People rarely develop foot ulcers when they have intact peripheral sensation. Due to the lack of painful feedback, peripheral neuropathy allows an environment where an injury can occur that is not recognised by the patient. This results in a person being able to wear a hole in the bottom of his or her foot just as one might wear a hole in a stocking (19). It is the constant repetitive stress that, in the face of neuropathy, leads to failure of the tissue and ultimately ulceration 20, 21, 22).

Identification of and diagnosing a patient with peripheral neuropathy is a critical task in screening and risk stratification among persons with diabetes. Many studies have been conducted attempting to define methods of testing for neuropathy and determining the point of neuropathy. Several studies have shown that the 10‐g Semmes–Weinstein monofilament (SWMF) is one of the most effective instruments to screen persons with diabetes. The instrument is inexpensive and reusable. The test is non invasive, reproducible and easy to perform by a physician or nurse. Inability to feel of four or more out of ten sites on the bottom of the foot using the SWMF carried with it a 97% sensitivity and a 83% specificity (23). When the SWMF is combined with a vibration perception examination, the sensitivity rose to 100% with a specificity of 77%. Furthermore, a combination of one or more positive questions on a focused neuropathy symptom score coupled with four out of ten imperceptible sites imperceptible to the SWMF yielded a 97% specificity and 86% specificity. It should be noted, however, that the SWMF is not a perfect tool. In fact, differences in design and manufacture can lead to dramatic differences in sensitivity and specificity. Furthermore, the device becomes more pliable and therefore oversensitive if used repetitively throughout the day. It is therefore recommended that several devices be rotated throughout the day to avoid overdiagnosing loss of protective sensation (24, 25). As there are no readily available clinical devices that can simultaneously evaluate large and small fiber neuropathy, it is probably prudent for the specialists to consider combining modalities (26).

History of ulceration

A history significant for ulceration or amputation heightens the risk of further ulceration, infection and subsequent amputation. This is due to abnormal distribution of plantar pressures that are often the cause of ulceration and that are often encountered following an amputation (27). It may be assumed that patients with a history of ulceration possess all the risk factors necessary to produce another ulceration. It is therefore not surprising that between 20% and 58% of patients develop another ulcer within a year after healing a wound (28, 29).

Structural deformity

There are two main mechanisms by which foot deformity and neuropathy bring about skin breakdown. The first mechanism refers to prolonged low pressure over a small radius of curvature. In this scenario, a prominent foot deformity such as a bunion or hammertoe deformity rubs against the shoe. The unrecognised pressure and shear forces over the deformity generally cause wounds over the medial, lateral and dorsal prominences of the forefoot. The second and most common mechanism involves prolonged repetitive moderate stress. This normally occurs on the ball of the foot and is thought to be associated with prominent metatarsal heads with a displaced or atrophied fat pad. Foot deformities are believed to be more common in the persons with diabetes due to atrophy of the intrinsic musculature associated with motor neuropathy. The intrinsic musculature of the foot functions to stabilise the toes during gait. In the presence of neuropathy, the lesser digits tend to contract and form hammertoes. The metatarsophalangeal joints tend to sublux and dislocate, which increase the prominence of the metatarsal heads and anteriorly displace the fat pad that normally dissipates stresses directly under the ball of the foot (30, 31). Rigid deformities and/or limited range of motion at the subtalar or metatarsophalangeal joints have also been associated with the development of diabetic foot ulcers (32, 33). Decrease in joint mobility has been observed in the hand, foot and ankle of persons with diabetes and associated with soft tissue glycosylation (34, 35). Decreased motion in weight‐bearing joints increases the load on adjacent joints and interrupts the normal transfer of pressures that occur on the foot during normal ambulation (36).

Additional, more complex deformities may also be present on a screening examination. The most widely recognised of these is the so‐called ‘rocker bottom’ foot caused by Charcot arthropathy. This deformity, which is thought to be caused by a combination of large and small fibre peripheral neuropathy, relatively good vascular outflow and repetitive stress or a single (often unrecognised) traumatic event in the at‐risk patient, can lead to profound swelling and bony deformity. Its incidence appears to be similar to that of lower extremity amputations in the US (3). This deformity often occurs in the arch area due to a combination of plantarflexory pull from the Achilles tendon and elevated plantar pressure, causing dislocation in the midfoot (33, 37). Charcot arthropathy of the foot should be included in the differential diagnosis of a patient presenting with a red, hot, swollen foot, particularly in the absence of any open wound (38).

Poor metabolic control

Poor systemic control of blood glucose is associated with a host of systemic complications. These include neuropathy (39), impaired white blood cell function (40, 41), soft tissue cross‐linking through production of advanced glycosylation products (42) and ulceration (43). In a direct sense, this cross‐linking can make the skin more friable and more prone to repetitive stress injury (44). Aggressive metabolic control with appropriate lower extremity care may reduce overall risk for ulceration and amputation (14).

Are risk factors of ulceration cumulative?

It has been reported that neuropathy, deformity, high plantar pressure, poor glucose control and male gender are significant risk factors of ulceration in diabetic patients. Additionally, it has also been noted that these risks are cumulative. Patients with neuropathy alone are at approximately 1·7 times greater risk of presenting with ulceration than patients without neuropathy. This risk increases to 12·1 times when patients present with neuropathy and deformity. Patients with neuropathy, deformity and a history of ulcer or amputation are at approximately 36 times greater risk of developing another ulcer (14). These evidence‐based categories and corresponding treatment strategies are essentially incorporated into the International Working Group Classification for diabetic foot risk (Table 1) (45, 46).

Table 1.

International Working Group Classification of diabetic foot risk (44)

Grade 0	No neuropathy present
Grade 1	Neuropathy without deformity or history of ulceration
Grade 2	Neuropathy with deformity or peripheral vascular disease
Grade 3	History of ulcer, amputation

While classifying basic risk of ulceration is important, one must also be adept in describing and classifying a pre‐existing wound. There have been numerous wound classification systems proposed and utilised 47, 48, 49, 50, 51). Unfortunately, few have concisely and consistently included the three key factors associated with risk of amputation. These three key factors can be summed up as depth, infection and ischaemia (47). Presently, the most validated system used that includes these factors consistently is the system proposed by the University of Texas (Table 2) (52). While there are other systems either in place or in development that address these issues, it seems a logical starting point to use this system for purposes of discussion. Again, there are three key questions to ask when assessing a wound.

Table 2.

The University of Texas Diabetic Wound Classification System (46, 51)

	Grade
Stage	0	1	2	3
A	Preulcerative or postulcerativelesion completely epithelialised	Superficial wound not involvingtendon, capsule or bone	Wound penetrating to tendonor capsule	Wound penetrating to bone or joint
B	Preulcerative or postulcerativelesion completely epithelialisedwith infection	Superficial wound not involvingtendon, capsule or bonewith infection	Wound penetrating to tendonor capsule with infection	Wound penetrating to bone or jointwith infection
C	Preulcerative or postulcerativelesion completely epithelialisedwith ischaemia	Superficial wound not involvingtendon, capsule or bonewith ischaemia	Wound penetrating to tendonor capsule with ischaemia	Wound penetrating to bone or jointwith ischaemia
D	Preulcerative or postulcerativelesion completely epithelialisedwith infection and ischaemia	Superficial wound not involvingtendon, capsule or bone withinfection and ischaemia	Wound penetrating to tendonor capsule with infection andischaemia	Wound penetrating to bone or jointwith infection and ischaemia

1. How deep is it?

Depth of the wound and involvement of underlying structures are the most commonly utilised descriptors in wound classification. Wounds are graded by depth. Grade 0 represents a preulcerative or postulcerative site. Grade 1 wounds are superficial wounds through the epidermis or epidermis and dermis but do not penetrate to tendon, capsule or bone (Figure 1). Grade 2 wounds penetrate to tendon or capsule. Grade 3 wounds penetrate to bone or into a joint. We have known for some time that wounds that penetrate to bone are highly prone to osteomyelitis (53). Additionally, we have observed that morbid outcomes are intimately associated with progressive wound depth. When this question is answered and graded as 0, 1, 2 or 3, we may then move on to the wound's stage, which is divided into four groups (clean, infected, ischaemic and both infected and ischaemic).

Figure 1.

Superficial diabetic foot wound.

2. Is infection present?

The definition of infection is not an easy one. Cultures, laboratory values and subjective symptoms are all helpful. However, the diagnosis of an infection's genesis and resolution has to be, and continues to be, a clinical one (4). The presence of purulent exudate and/or local signs of inflammation, sinus tract formation, fluctuance or crepitation may be highly indicative of infection (54, 55). However, it is important to note that, due to often‐profound loss of protective sensation, pain is not always noted with infected diabetic foot ulcers (56). Furthermore, while systemic signs and symptoms of sepsis should provide important cues to the treating clinician, they are frequently absent in persons with even significant diabetic foot infections 57, 58, 59). While criteria for infection may be something less than clear‐cut, there is little question that presence of infection is a prime cause of lower extremity morbidity and frequently develops into gangrene and subsequent amputation. Nonetheless, if a wound is clean, it falls into stage A. If it is infected, it falls into stage B.

3. Is it ischaemic?

The condition of ischaemia in tissue often results in amputation (6). Few other qualitative factors can necessitate amputation alone. Neuropathy and wound depth are not stand‐alone factors for the need for amputation of an affected limb; to generate an infection, one must frequently have an open wound. Therefore, the identification of ischaemia is of the utmost importance when evaluating a wound. If pulses are not palpable, or if a wound is sluggish to heal even in the face of appropriate off‐loading and local wound care, appropriate non invasive vascular studies are warranted followed by a prompt vascular surgery consultation and possible intervention to improve perfusion and thereby effect healing. Recent guidelines have suggested that regular screening for vascular disease through the use of ankle‐brachial systolic pressure index (ABI) may be of benefit for not only identifying peripheral ischaemia, but also potentially for identifying risk of cardiovascular morbidity and mortality if it is either low (<0·9) or high (>1·4) 60, 61, 62). While the ABI may not be sensitive enough to detect subtle signs of ischaemia, it might be useful as an initial measure prior to embarking on further investigations if there is a clinical index of suspicion. Regardless of what type of assessment is used to initially assess for ischaemia, it is clearly a risk factor for poor healing. If a wound is ischaemic, it falls into stage C (Figure 2). If the wound is both infected and ischaemic, it is categorised into stage D.

Figure 2.

Mummifying second digit secondary to ischaemia.

Once these three questions are accomplished, a wound may be classified based on the above listed criteria. For instance, an infected wound that probes to tendon with no bone involvement and adequate blood flow would be termed a UT grade 2B wound. When the infection is resolved by appropriate medical care, the wound classification would be revised to 2A.

Subsequent to the appropriate diagnosis of and classification of a diabetic neuropathic ulceration, treatment may then commence. A plethora of treatment modalities exist and few physicians would attempt to state that there is one treatment that may be used successfully on all wounds. What is paramount is that proper wound care tenets be observed. These include appropriate debridement of necrotic and undermining tissue and reduction of pressure through offloading of the diabetic foot wound (63).

In conclusion, it is observed that many of the most common component causes for neuropathic ulceration, infection and subsequent amputation may be identified using simple, inexpensive equipment in a primary care setting (Table 3). However, to initiate treatment based on the information gathered, a thorough knowledge of the risk factors' interactions and cumulative effect are of paramount important. Also of critical import is the appropriate communication of these risk factors to other members of the diabetic limb salvage team. Only when these goals have been met will we be able to make a meaningful long‐term, widespread impact on the unnecessarily high prevalence of diabetes‐related lower extremity amputations both in our nation and throughout the industrialised world.

Table 3.

Three key, take‐home messages for appropriate assessment of the diabetic foot

1.	Persons with diabetes should have their shoes and socks removed on every visit to the family physician to facilitate a brief, focused assessment.
2.	The key risk factors for most diabetic foot wounds include neuropathy, deformity and repetitive stress. Ischaemia is a critical factor but is generally considered a risk factor for not healing a wound and subsequent amputation.
3.	The key risk factors associated with a poor prognosis when an ulcer is present are depth, infection and ischaemia. These should be evaluated whenever assessing a wound.