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VASCULAR SURGERY e II

Foot complications in The foot in diabetes


Patients with diabetes are at risk of developing multiple com-
patients with diabetes plications making their feet susceptible to damage. The triad of
neuropathy, ischaemia and infection interact to cause tissue
Clifford P Shearman damage which if neglected leads to amputation. Patients with
neuropathy are also prone to develop Charcot neuroarthropathy,
Nandita Pal
an uncommon complication which may manifest as a unilateral
hot swollen foot (see below).

Abstract
Foot complications are a common cause of hospital admission of patients
Neuropathy
with diabetes and a frequent cause of amputation. Neuropathy and arte-
Diabetic polyneuropathy is one of the commonest complications
rial disease make the foot particularly vulnerable, but infection is often
of diabetes, affecting the feet of at least 28% of diabetics. The
the final presenting complication. Recognition of the patient at risk may
exact aetiology of the neuropathy is unclear but it is closely
prevent the development of foot complications initially, but if they
linked to the duration of diabetes, the adequacy of glycaemic
occur urgent treatment is required to prevent limb loss. The infected
control and the presence of retinopathy and nephropathy. Neu-
foot in a patient with diabetes is a surgical emergency. In addition to an-
ropathy affects sensory, motor and autonomic nerves, each of
tibiotics, debridement and surgical drainage of infection should be
which has deleterious consequences for the foot.
considered within the first 24 hours. Once the foot is made safe revascu-
Sensory neuropathy: this results in loss of protective sensation
larization should be undertaken in those with significant arterial disease.
allowing injury to go unnoticed. More commonly chronic repet-
Adoption of a multidisciplinary team approach to managing diabetic foot
itive injury, often from inappropriate foot wear, is not noticed
complications has resulted in reduction in major amputation in some
until tissue breakdown occurs. Loss of proprioception has
European countries.
negative effects on gait even at rest. Loss of the normally subtle,
but protective changes in biomechanical load distribution, can
Keywords Diabetic foot disease; diabetic vascular disease; foot com-
result in sustained stress and tissue damage. In some patients
plications of diabetes
sensory nerve damage results in pain or allodynia (perception of
pain on light touch).

Motor neuropathy: diabetic neuropathy predominantly affects


Epidemiology the small peripheral nerves. The intrinsic muscles of the foot,
Diabetes affects approximately 3% of the UK population. Hos- predominantly flexors, are affected more than the extensor
pital costs of treating diabetic complications are approximately groups in the calf. This in-balance results in clawing of the toes
9% of total NHS hospital costs. Foot complications account for and prominence of the metatarsal heads, with loss of the pro-
more admissions than any other diabetic complication, costing tective plantar fat pads. The foot is very prone to injury from
around £650 million in 2010e2011 in England. both friction by foot wear and abnormal weight distribution
Each year 5% of patients with diabetes will develop a foot (Figure 1). The first clinical sign is callus formation which is
ulcer, the lifetime risk being 15%. Most foot ulcers heal with rigid, causing even greater pressure on the tissue beneath. Callus
appropriate care but 25% recur. The development of a diabetic may crack and fissure providing a portal of entry for infection.
foot ulcer is a major prognostic indicator, preceding more than
80% of lower limb amputations in the UK. Diabetes is the com- Autonomic neuropathy: loss of sweating occurs resulting in dry
monest cause of leg amputation worldwide and it poses a 13-fold skin that is prone to cracking and infection. Autonomic regula-
risk increase. tion of skin blood flow may be lost, increasing shunting through
Amputations in patients with diabetes could be avoided in up arterial venous fistulae, producing skin that feels warm and looks
to 85% of cases, with better foot care, glycaemic control and pink, but in fact has reduced nutritional blood supply.
patient education facilitated by a multidisciplinary team. Despite
this, in the UK, around 100 people a week lose a leg through
Ischaemia
diabetes, and the amputation rate is 2.7 per 1000 people with
Peripheral arterial disease (PAD): patients with diabetes have a
diabetes, with significant morbidity, and mortality rates
4-fold increased risk of developing lower limb peripheral arterial
approaching 50% at 2 years.
disease (PAD). Diabetes itself, is an independent prognostic risk
indicator, and amplifies the effect of other factors including
smoking, dyslipidaemia and hypertension. Patients with diabetes
Clifford P Shearman MS FRCS is Professor of Vascular Surgery at the and PAD have an excess risk of potentially avoidable cardio-
University of Southampton, Southampton, UK. Conflicts of interest: vascular events such as heart attack and stroke. In patients with
none declared. Type 1 diabetes, good diabetic control is associated with a 42%
reduction in cardiovascular events. The evidence for Type 2
Nandita Pal MD FRCS is a Specialist Registrar in Surgery, Wessex diabetes is unclear, however evidence is emerging of long-term
Deanery, UK. Conflicts of interest: none declared. cardiovascular benefit from good glycaemia control.

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VASCULAR SURGERY e II

Patients with known PAD are at greater risk of developing foot


ulcers and are frequently asymptomatic until they develop.
Reduced perfusion will impair wound healing and the response
to infection.

Microcirculation: the microcirculation is not directly affected by


atherosclerosis, but diabetes does affect the microcirculation in a
number of ways. There are vasomotor abnormalities which may
reduce capillary flow in the skin. There is thickening of vascular
endothelial cells, with associated increased permeability and
platelet aggregation. These observations help explain how
wounds which are healthy and bleeding at the time of surgery
can deteriorate and die back as the vessels in the microcircula-
tion thrombose.
It is important to appreciate how the effects of PAD are
compounded by microcirculatory abnormalities. What might
Figure 1 Foot of patient with diabetes. Dry, flaky skin due to the auto-
nomic neuropathy can be seen. The clawing of the toes secondary to the seem a relatively minor lesion in a large artery may, when
motor neuropathy which has resulted in rubbing of the toes and dorsum combined with microcirculatory impairment, reduce tissue
of the foot on the patient’s shoe, which he was unaware of due to reduced perfusion below a critical threshold.
sensation.
Infection
The immune response of patients with diabetes may be
Patients with Type 2 diabetes in particular are commonly abnormal. Neutrophil phagocytosis is impaired not only making
found to have associated hypertension, dyslipidaemia, hypothy- the patient with diabetes prone to infection but also may mask
roidism and obesity, termed metabolic syndrome. Smoking, the clinical response. Only about one-third of patients with foot
however, remains the most powerful predictor of the risk of infection will have a temperature, and the white cell count may
developing PAD. Correction or control of these factors signifi- not be elevated despite extensive infection.
cantly reduces cardiovascular mortality but is often omitted. It has been estimated that of patients with foot complications
PAD is caused by atherosclerosis but there is increasing evi- approximately 25e45% are due to neuropathy, 10% are due to
dence to suggest that the disease process in diabetic and non- ischaemia and 45e60% are neuro-ischaemic, a combination of
diabetic patients differs. Atherosclerotic plaque in patients with both. Infection is often the final common pathway to presenta-
diabetes contains more calcium and has increased expression of tion (Figure 3).
inflammatory markers, perhaps explaining the more aggressive
progression of the disease. Macroscopically the disease affects Charcot’s neuroarthropathy
more distal vessels, particularly in the calf and foot (Figure 2). This is an uncommon complication of diabetic neuropathy. It
Patients with diabetes are less likely to form collaterals after often follows minor trauma such as a sprain or fracture and the
vessel occlusion. foot becomes red, hot and swollen (Figure 4). It is a non-
infectious, acute inflammatory state with rapid destruction of
the foot bones. It can be difficult to distinguish from infection and

The relationship of neuropathy, ischaemia and a


mixture of both neuro-ischaemia
ISCHAEMIA
10%

INFECTION
Often final
presenting
complication

NEURO-ISCHAEMIC NEUROPATHIC
25–45% 45–60%

Based on work by Shaw and Boulton


Figure 2 Angiogram of patient with extensive peripheral arterial disease
affecting the calf arteries. Figure 3

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VASCULAR SURGERY e II

Figure 4 Charcot’s neuroarthropathy. A swollen red hot foot. A total con-


tact cast has recently been removed.

may be misdiagnosed, but the absence of a wound, marked


swelling and deformity should prompt the diagnosis and referral
to a specialist team. X-ray and magnetic resonance imaging
(MRI) scans may show bone destruction and in the absence of an Figure 5 CT angiogram of patient with peripheral arterial disease.
open wound this should suggest Charcot’s neuroarthropathy.
Treatment involves ‘offloading’ the foot mechanically, to
prevent further stress and injury. This can be achieved with total interpret and contrast media is nephrotoxic. Patients’ renal
contact casting or an AircastÒ. If, despite this, the foot continues function should be monitored and they should be well hydrated.
to deteriorate, surgical fixation is indicated. MR angiography is used but takes longer to obtain the images
and patients may find the scanner claustrophobic. Gadolinium is
Assessment used as a contrast agent and in patients with impaired renal
Vascular assessment function, is associated with systemic interstitial fibrosis, a
A history of cardiovascular disease increases likelihood of un- potentially fatal complication. Conventional angiography is
derlying arterial disease. Ulcers which are painful are more likely invasive and is normally reserved for selected patients.
to be ischaemic but neuropathy may mask this. Despite the
presence of arterial disease the foot may appear well perfused Neurological assessment
and warm due to autonomic neuropathy. Callus formation on weight bearing areas, and changes in foot
Palpation of pulses is vital. If in the presence of a foot lesion, shape are indicators of neuropathy. Dry cracked skin suggests
the limb pulses cannot be clearly felt then further investigation is autonomic involvement. Absence of sensation may not have
mandatory, even if pulse palpation is difficult due to deformity or been noticed by the patient, but the 10-g monofilament test to
oedema. Ankle blood pressures, measured using Doppler ultra- light touch on 10 sites in the foot or a 128-Hz tuning fork on the
sound, are useful in many patients with diabetes. If reduced, great toe to assess sensation vibration can be used to identify
compared to the brachial pressure (ankle brachial pressure index neuropathy in the majority of patients.
or ABPI of <0.9), PAD is likely. Patients with diabetes may have
Wound assessment
calcified, incompressible lower limb blood vessels, artefactually
Careful wound assessment to determine the depth and involvement
raising the measured ankle pressure. If there is any doubt it is
of deep structures such as bone, tendon and joints must be under-
possible to simply elevate the limb while insonating the ankle
taken. This can be done by clinical examination and probing the
vessels with the Doppler probe. If the signal disappears on
wound for bone in the wound base. Palpation may elicit a discharge
elevation, because the perfusion pressure of the limb has been
of pus which has tracked up the tendon sheaths. Plain X-rays will
exceeded, and reappears on lowering the limb this suggests se-
often reveal bone destruction due to long standing osteomyelitis,
vere circulatory impairment.
but may not detect early changes. MRI can be useful in evaluating
If there is any doubt about the limb circulation, an arterial
osteomyelitis and soft tissue infection, with a sensitivity of 90% and
duplex ultrasound scan should be performed. This is readily
specificity of 83%, and preoperatively can help plan the extent of
available, inexpensive, non-invasive and can clearly identify
resection required. Foot ulcers may be classified using the widely
areas of arterial disease.
used Texas Wound Classification System (Table 2).
Duplex ultrasound may be adequate to plan treatment in some
patients but more detailed imaging may be required, especially in
Management
blood vessels above the groin. CT angiography can give clear
pictures of the vessels and is relatively non-invasive (Figure 5), The management of patients with diabetes, at risk of foot com-
although the appearance of calcification can be difficult to plications, demonstrates the need for seamless working across

SURGERY 31:5 242 Ó 2013 Elsevier Ltd. All rights reserved.


VASCULAR SURGERY e II

Advice about foot care such as regular foot inspection and hy-
Identifying the foot at risk in patients with diabetes e giene, together with treatment of factors such as callus or fungal
NICE guidelines (2004) infection may prevent deterioration and is a vital aspect of care at
this stage. Checking that cardiovascular risk factors have been
Risk level Features Action
modified is essential.
Low risk Normal sensation Education and annual review
Management of the patient with a foot ulcer
Palpable foot pulses
Once an ulcer has developed then the underlying factors
Increased Neuropathy or Refer to specialist foot team
contributing to it must be identified and corrected. This may be
risk absent pulses Review 3e6 monthly
done electively, but often the patient will present as an emer-
High risk Neuropathy or Refer specialist foot team
gency. Management should be undertaken by a multidisciplinary
absent pulses Review 1e3 monthly
foot care team and can be divided into immediate, secondary and
Foot deformity
prolonged or continuing care (Figure 7).
Skin changes
Previous ulcer
Immediate treatment (within 4 hours of admission): infection is
Foot ulcer Urgent assessment within
the most common cause of acute presentation. The patient may be
24 hours by multidisciplinary
unaware of the extent or severity of infection due to impaired pain
team
sensation, poor vision and lack of systemic response. White cell
count and inflammatory markers may be normal in these patients,
Table 1
and deranged glycaemic control may be the only indicator of
infection. Infection in the foot of a patient with diabetes must be
both primary and secondary care. The multidisciplinary team treated as a surgical emergency. Usually if the infection is anything
should include podiatrists, specialist nurses, diabetic physicians, more than superficial, hospital admission is required.
general practitioners, vascular and orthopaedic surgeons, or- Blood glucose should be checked and the patient’s metabolic
thotists and microbiologists. There should be a clear pathway of state brought under control with intravenous fluids and an in-
care agreed by all those involved and the roles of each member of sulin sliding scale if necessary. Cultures from open wounds or
the team defined. from deep tissue by aspiration of tissue fluid should be obtained.
Management of the foot in diabetes can be divided into care The ulcer should be gently probed to assess for osteomyelitis.
for people with no foot lesion and those who have developed an Broad-spectrum intravenous antibiotics should be commenced
ulcer. For the latter group care can be divided into immediate according to local protocols.
care, second phase care for those admitted to hospital, and Careful assessment of the foot must be undertaken by an
continuing care. experienced clinician. Plain X-rays of the foot may show osteo-
myelitis, and gas in the tissues demonstrates the extent of the
Management of the person with diabetes but no foot ulcer infection (Figure 6).
Many patients with diabetes have a risk of foot complications In patients with evidence of deep-seated infection, or exten-
similar to the normal population. Annual screening will identify sive infected necrotic tissue, surgical debridement and drainage
those patients at risk of foot ulceration (Table 1), and early should be undertaken as soon as the patient is fit for surgery,
problems such as callus formation or erythema due to poor foot but certainly within 24 hours. Removing devitalized tissue and
wear can be corrected by an experienced podiatrist before sig- draining infected compartments will prevent further necrosis and
nificant tissue damage occurs. If an ulcer occurs, expeditious make the condition safe. Tissue from deep layers should be sent
wound care and offloading the damaged area with orthotics will for microbiological culture, and wounds left open for later revi-
prevent deterioration and allow healing. sion or to heal by secondary intention.
Patients who have been identified to be at increased risk need Rarely if the patient is systemically unwell with extensive limb
to be reviewed regularly by a clinician with expertise in the field. infection and not responding to initial treatment, amputation has

The Texas Wound Classification System. The depth of the wound and involvement of deeper structures is assessed. The
presence of infection, ischaemia or both then determines the score
0 I II III

A Pre- or post-ulcer: lesion Superficial wound, not involving Wound penetrating to Wound penetrating to
completely epithelialized tendon, joint capsule or bone tendon or joint capsule bone or joint
B þinfection þinfection þinfection þinfection
C þischaemia þischaemia þischaemia þischaemia
D þischaemia and infection þischaemia and infection þischaemia and infection þischaemia and infection

Table 2

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VASCULAR SURGERY e II

Acute diabetic foot


Refer to MDT within 24 hours
Ulceration/inflammation/infection
Deformity/arthropathy
Ischaemia/gangrene

Clinical assessment
Local/systemic infection
Limb ischaemia

Investigations
Bloods – WBC/Inflam markers
Imaging – X-ray/MRI
Microbiology samples

Acute management
Antibiotics
Surgical debridement
Revascularization

Continuing care with MDT


Co-morbidities – cardiovascular/renal
Wound management
Vascular assessment
Orthotic assessment
Foot deformity
Figure 6 Plain X-ray of infected foot showing extensive gas in the tissues
Treat minor infection
around the fifth toe.
Coordinate primary and community care

MDT, multidisciplinary team; WBC, white blood cells.


to be undertaken as a life-saving measure. In these situations a
guillotine amputation is preferred, removing all infected material
Figure 7 Management pathway for acute diabetic foot disease for patients
and the amputation revised later when the patient is well. admitted to hospital.

Second phase treatment (4e48 hours of admission): after


initial management, investigations and response to treatments prevent adequate drainage of infection and puts extra pressure
should be assessed, and referral to a specialist team should be on the wound edge, risking necrosis. A number of dressings are
made within 24 hours of admission. used, but there is little strong evidence to support one over
In patients with advanced ischaemia the need to revascularize another. Negative pressure wound therapy, however, has made a
the limb may be obvious but in those with mild to moderate PAD major contribution to managing foot wounds. There is evidence
and reasonable perfusion of the foot it can be difficult. Skin that it increases the rate of wound healing and portable devices
transcutaneous oxygen tension measurements on the foot may permit an early return to the home environment. Negative
provide prognostic information for wound healing. Tissue pressure therapy has been particularly useful for ulcers over the
bleeding at the time of surgery and early appearances of the calcaneum. Larval therapy has been advocated in the non-
wound may aid the decision. In principle it is rare for an exten- healing wound with little evidence. Hyperbaric oxygen therapy,
sive foot wound to heal in a patient with diabetes unless perfu- growth factors and dermal and skin substitutes should only be
sion is good. Early revascularization results in improved healing used as part of a clinical trial.
and should be considered in any patient in whom there is doubt For extensive tissue loss in patients with good blood supply
about the limb circulation. more complex reconstructions should be considered including
Based on extent of the disease, blood supply can be improved free tissue transfer.
by open surgery (bypass, endarterectomy) or endovascular Offloading the foot wound is essential. In the early stages this
treatments (angioplasty). The majority of patients with diabetes can be achieved by bed rest which also reduces oedema which
will require an infra-inguinal procedure and there appears to be inhibits healing. Care needs to be taken to avoid the development
little difference in limb salvage between the two approaches. of new pressure related ulcers and to use DVT prophylaxis. Early
Endovascular treatments are less invasive and hospital stay is mobilization can be achieved using AircastsÒ or total contact
shorter but surgical treatments may confer a longer-term benefit. casts.

Wound care: it is generally better to let surgical wounds on the Amputations: these remain one of the most feared complications
foot heal by secondary intention. Suturing the wound may of diabetes and can have devastating consequences for the

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VASCULAR SURGERY e II

individual patient in terms of quality of life, but also wider im- Encouragingly there is evidence from a number of other
plications in terms of cost to the NHS and society. Around 6000 European countries such as Finland that implementation of clear
people with diabetes undergo major (leg) and minor (foot and policies to identify patients at risk and to intervene early in those
digit) amputations in England each year. The incidence of major who develop complications can have a major impact on hospital
amputations is around 2.7 per 1000 people with diabetes, but admission and major amputation rates. A
varies 10-fold across different regions in England. This may in
part be due to varying involvement of multidisciplinary teams in
decision making. There is growing evidence that reductions in FURTHER READING
amputation rates can be achieved following the introduction of Boulton AJM, Vileikyte L, Ragnarson-Tennvall, Aplevist J. The global
multidisciplinary teams, and this has been emphasized by the burden of diabetic foot disease. Lancet 2005; 366: 1719e24.
‘Putting Feet First’ report, and the NICE guidance on ‘Inpatient Diabetic foot problems: inpatient management of diabetic foot problems.
management of diabetic foot problems’. NICE Clinical Guidance 2011; 119.
Holman N, Young RJ, Jeffcoate WJ. Variation in the recorded incidence of
Continuing care and prevention: when a patient leaves hospital amputation of the lower limb in England. Diabetologia 2012; 55: 1919e25.
it is essential to ensure that they are aware of the risks of further International Diabetes Federation. Position statement e the diabetic foot,
foot problems and take precautions to avoid them. Appropriate 2005. http://www.idf.org/Positionstatementsdiabeticfoot.
foot wear, access to regular follow up and a point of contact if Jeffcoate, Edmonds M, Rayman G, Shearman C, Stuart L, Turner B. Putting
there is deterioration are all important. If the patient has suffered feet first e national guidance at last. Diabet Med 2009; 26: 1081e2.
an amputation then advice and care are needed to prevent Veves A, Giurini JM, LoGerfo FW, eds. The diabetic foot. Medical and
problems with the remaining foot. surgical management. Totowa, New Jersey: Humana Press, 2002.

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