Professional Documents
Culture Documents
Wound 2021 0016
Wound 2021 0016
ª David Dayya et al., 2021; Published by Mary Ann Liebert, Inc. This Open Access article is dis-
tributed under the terms of the Creative Commons License [CC-BY] (http://creativecommons.org/
licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, pro-
vided the original work is properly cited.
devoid of normal blood supply promote an inflam- process of wound healing is impaired and the wound
matory phase environment. This inflammatory progresses, then the risks of infection, amputation,
phase of healing is evidenced by an abundance morbidity, and mortality increase.3
of inflammatory cells and inflammatory media- Foot ulceration affects 15–34% of diabetics at
tors. This inflammatory phase includes an increase some point in their lives.4–6 The prevalence of di-
in the enzyme matrix metalloprotease and inflam- abetes is estimated to include 7% (4.8 million) in
matory cytokines that facilitate inflammatory cel- the United Kingdom, 9.4% (30.3 million) in the
lular opsonization and chemotaxis. This phase of United States, and 7% (366 million) of the world’s
healing attracts additional inflammatory cells and population.5,7 These figures suggest the prevalence
continues this repetitive detrimental cycle. of DFUs afflict up to 1.6 million in the United
Kingdom, 10.3 million in the United States, 124
CLINICAL RELEVANCE million of the world’s population. Debridement is
regarded as an effective intervention to accelerate
Understanding the complicating factors that
ulcer healing and to decrease the risk of serious
delay wound healing at the mechanistic level of
complications.8
healing, including at the biochemical, cellular, and
tissue level warrants the need to remove devitalized
Global data reports
tissue from a DFU at the clinical level. Debridement
In 2009 the International Working Group on
helps limit the growth of pathologic organisms
the Diabetic Foot (IWGDF) began its efforts to pro-
and tempers the inflammatory response that stag-
duce consensus guidelines on the diabetic foot.9 In
nates the DFU in the inflammatory phase of heal-
2011 the IWGDF estimated that of the worldwide
ing. Debridement effectively returns the wound to
7.0% (366 million) of individuals with diabetes,
the initial acute wound phase of healing, or the
80% (292 million) reside in developing countries.9
hemostasis/coagulation phase of healing. Debride-
The IWGDF 2012 estimated that by the year
ment promotes the progression of the DFU to ad-
2030 there will be 8% (552 million) individuals
vance through the stages of wound healing from the
globally who are afflicted with diabetes (Type 1/
hemostasis/coagulation phase through the matu-
Type 2) in the adult population.10 Annually greater
ration phase of healing. The removal of devitalized
than 1 million people undergo a limb amputation,
tissues is critical in promoting angiogenesis, vas-
or one amputation occurs every 30 s.9 The preva-
culogenesis, and the development of granulation
lence of DFUs is estimated to be 19% to 34%,
tissue, which facilitates healing in an accelerated
whereas the recurrence rate of DFUs is estimated
time frame and prepares the wound bed for addi-
to be 40% within a year and 65% within 3 years.1
tional intervention measures. There are a variety of
The majority of amputations are preceded by a foot
debridement methods that are broadly grouped into
ulcer and the IWGDF 2019 estimates that after a
two primary categories, including nonmechanical
major amputation up to one half of this group will
and mechanical debridement. Our review focuses
die within 5 years.1
on the science surrounding debridement of DFUs
The most important risk factors involved in the
and both categories of debridement modalities.
development of these ulcers include peripheral
neuropathy, foot deformities, minor foot trauma,
INTRODUCTION and peripheral arterial disease (PAD) (Figs. 1–3).
The DFU is defined in accordance with the Once the ulcer appears, infection and PAD are
International Working Group on the Diabetic Foot considered major causes leading to amputation.
(IWGDF) as a break of the skin of the foot that The burden of amputations in developing coun-
includes minimally the epidermis and part of the tries is greater than it is in developed countries.
dermis, in a person with DM, this may be associated The working group estimated that *28–50% may
with infection, ulceration, or destruction of tissues progress to the point where they require amputa-
of the foot associated with neuropathy and/or pe- tion (major or minor).1,9–11
ripheral artery disease in the lower extremity.1 The There is significant psychosocial impact in peo-
ulcer is the result of a break in the dermal barrier, ple with DFUs, including those who have required
with subsequent erosion of underlying subcutane- amputations. Frequently comorbid depression and
ous tissue. In severe cases, the breach may be ex- a reduced quality of life result in an increase in
tended to muscle and bone. The progression to ‘‘social isolation.’’12,13 Chronic psychosocial stress
ulceration may be attributed to an impaired arterial can have immunocompromising effects.14 The risk
blood supply, neuropathy, musculoskeletal defor- of amputation is increased in these individuals
mities, or a combination of these factors.2 If the living alone, and lacking in social support. Timely
668 DAYYA ET AL.
Figure 2. Serial images depicting measurements of Wagner grade 2 wound with progressive healing clockwise in this diabetic (A–C) patient using a
combination of offloading and sequential debridement’s lasting 12 weeks, including a combination of sharp, enzymatic, and autolytic.
For comparison of the results, costs were first adjusted for inflation to 2005 prices with the consumer price index f and then converted to USD with the
appropriate currency exchange rate for 2005. (Please note: U.S. Department of Labor and Statistics Inflation Calculations were used and are in brackets below
the 2005 costs to make the conversion to compare to 2/2021 cost equivalency.)
Please note that the above table is a compilation of studies investigating costs associated with treating leg and foot wounds in diabetics was developed by
the IWGDF; however, these costs may include costs incurred for treating wounds other than diabetic foot ulcers, but can also be associated with diabetics
such as ischemic ulcers, pressure ulcers, and venous stasis ulcers.
A table displaying data from IWGDF 2012 (Reproduced here with permission from the IWGDF).
a
Based on data from observational studies.
b
Based on data from databases and other secondary sources.
c
Number of episodes.
d
Includes 80 amputations.
e
Number of hospitalizations.
f
Outpatient costs are direct medical costs incurred by patients receiving ambulatory care.
g
Inpatient costs are direct medical costs incurred as a result of care rendered in the course of hospitalization.
IWGDF, International Working Group on the Diabetic Foot; LEA, lower extremity amputation; Major, amputation above the ankle; Minor, amputation below the
ankle; NA, not applicable.
syndrome is defined according to the International Foot-related problems may use 12–15% of
Diabetes Federation (IDF) as38: health care resources for diabetes in the developed
world, whereas in developing countries this may
(1) Central obesity with waist circumference
be as high as 40% (see Table 1 above).1,9,10
with ethnicity specific values plus ANY 2 of
Global estimates of direct and indirect costs in-
the following four factors.
clude a global economic burden that will increase
(i) Raised triglycerides ‡150 mg/dL, or spe- from $1.3 trillion to $2.2 trillion by 2030 in U.S
cific treatment for this lipid abnormality. currency. This increase in costs as a shared global
(ii) Reduced HDL Cholesterol <40 mg/dL in GDP is estimated to rise from 1.8% in 2015 to a
males OR <50 mg/dL in females OR spe- maximum of 2.2% by 2030.39
cific treatment for this lipid abnormality. The estimated total cost of diabetes, including
(iii) Raised blood pressure ‡130 mm Hg systolic direct and indirect costs in the United States in
OR ‡85 mm Hg diastolic OR treatment of 2017 was $327 billion.40,41 This included a direct
previously diagnosed hypertension. cost of $237 billion and an indirect cost of $90 bil-
(iv) Raised fasting plasma glucose >100 mg/ lion. Direct costs include medical costs, such as
dL OR previously diagnosed Type 2 DM. inpatient visits, emergency department visits, out-
patient visits, prescription drugs, medical equip-
Estimated costs ment, and home health services. Whereas indirect
Global cost estimates. The IWGDF has issued costs primarily relate to nonmedical costs, such as
a report on the cost of DFUs and amputations lost productivity, wages, work absence, and travel
(Table 1). expenses, associated with receiving treatment.
DEBRIDEMENT OF DIABETIC FOOT ULCERS 671
The peak age-range for amputations is between arterial insufficiency), and poor nutritional status
41 and 70 years, a time period of prime working (inadequate protein/nutrients required for wound
age and productivity for adults.24 This poses a sig- healing). It is believed that these combined problems
nificant health challenge to our workforce since contribute to the wound stagnating within the in-
amputations can result in permanent impairment flammatory phase of the healing process. The de-
often qualifying an individual for disability benefits velopment of a wound involves minor soft tissue
resulting in lost wages and productivity.42 This po- injury or insult compounded by these factors. The
ses a significant stress on the family unit. It imposes trauma can be the result of friction, mechanical
an economic burden upon society at large in pro- shearing forces, direct pressure, or penetrating tis-
viding for impaired and disabled individuals. The sue injury, including sharp or blunt trauma.3,48,49
rate of amputations is rising and these factors are
directly contributing to this alarming trend.7,15,26 Vascular insufficiency. Diseases of blood ves-
The U.S. Government estimates for the 2017 sels, including arterial and venous, whether mac-
GDP portion allocated for direct health care costs rovascular or microvascular are a major cause
was $2.2 trillion or 16% of the GDP.43 Chronic of complications in diabetes and can complicate
diseases, including heart disease, stroke, cancer, wound healing of DFUs.50 The Framingham study
and diabetes, cause 7 out of 10 deaths and are re- reported that more than 50% of men and women
sponsible for 75% of the $2 trillion spent on health with diabetes had absent foot pulses.51 The Fra-
care.44 In comparison, the direct and indirect mingham study is in its third generation of parti-
costs for diabetes in 2007 was *10% of 2.2 trillion cipants and comprises a total of 4,095 people.52
dollars. Up to 15% of costs for DM in the devel- PAD tends to occur at younger ages in people
oped world is estimated to be allocated for foot- with diabetes and is believed to involve smaller
related problems, *33 billion dollars in the United blood vessels and capillaries. Reports from United
States.10,45 States, United Kingdom, and Finland concur that
The UK National Health Service (NHS) spends PAD is a major contributory factor in the patho-
an estimated £14 billion per year on diabetes or genesis of foot ulceration and subsequent major
11.7% of the NHS budget.46 Total direct and indi- amputations.53–56
rect costs for diabetes in the United Kingdom is Impaired blood flow can occur at both levels of
£23.7 billion per year.5 A report published in 2019 the microarterial and macroarterial circulation
estimates that the British NHS spends up to £1 in diabetics compounding the problem of delayed
billion spent on foot ulcers or amputations each wound healing from inadequate tissue oxygena-
year.46,47 tion and nutrients. Microcirculation involvement
includes the occlusion of small blood vessels and
Definition and description capillaries, whereas macroarterial insufficiency is
of the condition—DFUs defined as the occlusion of medium- and large-sized
Wound progression. The DFU is considered blood vessels.
multifactorial in its etiology. Wound repair and Hemodynamically significant macrovascular ar-
closure will help re-establish hemostasis, preserv- terial insufficiency is considered an advanced stage
ing the barrier function of the skin to prevent in- of PAD, which may warrant surgical revasculari-
fection, and maintaining the overall protective role zation procedures.57 These vascular occlusions and
of skin. the resulting wound hypoxia poses a major risk
Wound healing progresses through the follow- factor in the development of nonhealing problem
ing phases: (1) Hemostasis/Coagulation phase, (2) wounds.3,10,58 A host of considerations are believed
Inflammatory phase, (3) Proliferative phase, (4) to compound vascular insufficiency, which restricts
Maturation/Remodeling phase.3,48,49 the delivery of oxygen and nutrients required for
Problems with wound healing are considered adequate wound healing, immune function, and
multifactorial in diabetics. These prognostic factors can increase susceptibility of coinfections. These
may include the following: vascular insufficiency/ considerations may include nutritional status, car-
PAD, peripheral neuropathy (sensory/motor/ diovascular insufficiency, hydration status, psy-
autonomic), immunosuppression, and critical chosocial factors, smoking and alcohol history,
colonization/infection. patient compliance, socioeconomic status, availabil-
These problems may be more common in the ity of ancillary treatment modalities, proficiency
presence of nonviable tissue (contributing to in- and expertise of the health care provider involved
creased risk of infection and delayed wound heal- in the wound care, the type of wound, and the
ing), smoking (contributory to the risk of peripheral presence of wound occurrence from multifactorial
672 DAYYA ET AL.
wound mechanisms, the age of the patient, and microvascular insufficiency. Sensory function is
possibly the type of debridement method provided frequently tested using a 128 Hz tuning fork and
to the patient for removal of nonviable tissue from Semmes-Weinstein Monofilament.1
the wound bed and the periwound.3,9,10,59,60 Motor neuropathy. Denervation of muscles has
Venous insufficiency may delay wound healing direct effects on the function of the foot. The small
due to edema that increases the diffusion distance muscles of the foot, the extensor digitorum brevis,
for oxygen to travel from the arterial circulation lumbrical, and interosseous muscles are com-
across the tissue to the wound bed, and by com- monly affected.64 Paralysis of these small muscles
promising capillary diffusion through increased results in the metatarsophalangeal joints becom-
tissue hydrostatic impeding capillary flow.61 ing hyperextended and the interphalangeal joints
becoming flexed.62 The joints initially remain mo-
Neuropathy (sensory, motor, autonomic) bile, but later degenerative changes occur and the
Impairment of nerve function is an important joints become fixed.1,62
and frequent complication of diabetes. All types of The consequence of such muscle wastage is a foot
nerve fibers can be affected, including motor, sen- shape that increases foot pressures over bony
sory, and autonomic nerve fibers, and their func- prominences where wounds most commonly occur
tions. Impaired nerve function in the foot is in diabetics (Fig. 1).65
common in people with diabetes although the per-
Autonomic neuropathy. Autonomic neuropa-
son themselves may be unaware of its presence.
thy is thought to contribute to the pathogenesis
Neuropathy remains one of the major factors lead-
of ulceration, neuropathic edema, and Charcot
ing to the development of foot ulceration in people
arthropathy.1,62
with diabetes.62
Impairment of sweating contributes to the for-
Approximately 60–70% of diabetics have neuro-
mation of hyperkeratotic plaques and fissures in
logic disease, most often a peripheral neuropathy
the skin. Callus (increased glycation of keratin) be-
involving the lower extremities.7,15,26
comes thick, pressing on the soft tissues underneath
This microvascular disease component is beli-
contributing to ulceration.66 A callus defined as a
eved to cause occlusion within the vasa nervorum,
buildup of keratinized skin in reaction to persistent
which provides the blood supply to the nerves
pressure can exert pressure on the soft tissues of the
possibly due to the direct cytotoxic effect of the
foot.67 The dry cracking foot is a function of this
hyperglycemia.63 This form of microvascular oc-
neuropathy, anhidrosis, and impaired temperature
clusive disease contributes to the development of
regulation that contribute to these local effects.10
peripheral neuropathy. Since diabetic neuropa-
thy involves motor, sensory, and autonomic nerve Immunosuppression/critical colonization/
fibers, the pathologic deficits may include the infection
deformed, insensate, and dry cracking foot. Diabetes is considered an immunocompromising
condition. It has been observed that white blood
Sensory neuropathy. Damage to the nerves re- cells may behave atypically in a hyperglycemic en-
sponsible for conducting afferent sensory percep- vironment and do not marginate, migrate, or se-
tion from the foot renders the foot insensitive to crete the cytokines sufficiently that are required
temperature, vibration, pressure, and pain. These to combat infection.68 This can increase the risk of
are referred to as sensory neuropathy. The loss critical colonization and infection.
of sensation means that relatively minor injur- The immunosuppressive state that may occur
ies often go undetected and reinjury or repetitive in diabetics with an open wound can lead to critical
cumulative trauma can result in a wound that colonization and infection increasing the risks of
progressively worsens in severity. Repetitive cu- a nonhealing chronic wound.3,10,68 The chronicity of
mulative trauma can result from ill-fitting shoes this condition increases the risk of methicillin-
resulting in friction. The insensate foot, unlike a resistant Staphylococcus aureus (MRSA), which
normal innervated foot, does not warn the individ- is among the cultured organisms found in chronic
ual to make the needed adjustments or changes wounds and a major public health concern. Infections
required to arrest the insults responsible for that have reached the deeper bony level of tissue
wound progression and infection. The insensate involvement may become refractory to treatment.
foot does not result in the kind of vascular neu- The patient can be at risk for life-threatening sepsis
roregulatory changes required to supply the in- from a wound as the source of infection.3,10 This may
jured area sufficiently with oxygen and nutrients warrant urgent amputation to remove the source of
required for wound healing, which compounds the life-threatening sepsis.
DEBRIDEMENT OF DIABETIC FOOT ULCERS 673
0 1 2 3 4 5
No ulcer in a Wound involving full Wound extending to Wound with cellulitis Localized gangrene Extensive gangrene involving
high-risk foot skin thickness ligament and muscle or abscess the whole foot
674 DAYYA ET AL.
Grade
0 Pre- or Postulcerative lesion 1 Superficial wound not 2 Wound penetrating 3 Wound penetrating
Stage completely epithelialized involving tendon, muscle, or bone to tendon or capsule to bone or joint
A 0A 1A 2A 3A
No Infection, or ischemia
B 0B 1B 2B 3B
Infection but no ischemia
C 0C 1C 2C 3C
Ischemia but no infection
D 0D 1D 2D 3D
Infection and ischemia are present
W: Wound/clinical category
SVS grades for rest pain and wounds/tissue loss (ulcers and gangrene):
0 No ulcer No gangrene
Clinical description: ischemic rest pain (requires typical symptoms + ischemia grade 3); no wound.
Clinical description: minor tissue loss. Salvageable with simple digital amputation (1 or 2 digits) or skin coverage.
2 Deeper ulcer with exposed bone, joint or tendon; generally Gangrenous changes limited to digits
not involving the heel; shallow heel ulcer, without
calcaneal involvement
Clinical description: major tissue loss salvageable with multiple (‡3) digital amputations or standard TMA – skin coverage.
3 Extensive, deep ulcer involving forefoot and/or midfoot; deep, Extensive gangrene involving forefoot and/or midfoot; full
full-thickness heel ulcer – calcaneal involvement thickness heel necrosis – calcaneal involvement
Clinical description: extensive tissue loss salvageable only with a complex foot reconstruction or nontraditional TMA (Chopart or Lisfranc); flap coverage or complex wound
management needed for large soft tissue defect
I: Ischemia
Hemodynamics/perfusion: measure TP or TcPO2 if ABI incompressible (>1.3)
Patients with diabetes should have TP measurements. If arterial calcification precludes reliable ABI or TP measurements, ischemia should be documented by TcPO2, SPP, or
PVR. If TP and ABI measurements result in different grades, TP will be the primary determinant of ischemia grade.
Flat or minimally pulsatile forefoot PVR = grade 3.
ABI, Ankle–Brachial Index; PVR, pulse volume recording; SPP, skin perfusion pressure; TP, toe pressure; TcPO2, transcutaneous oximetry.
fI:
SVS grades 0 (none), 1 (mild), 2 (moderate), and 3 (severe: limb and/or life threatening)
SVS adaptation of Infectious Diseases Society of America (IDSA) and IWGDF perfusion, extent/size, depth/tissue loss, infection, sensation (PEDIS) classifications of diabetic
foot infection
(continued)
j 675
Table 4. (Continued )
Local infection involving only the skin and the subcutaneous tissue (without involvement of deeper tissues and 2 Moderate
without systemic signs as described below).
Exclude other causes of an inflammatory response of the skin (e.g., trauma, gout, acute Charcot neuro-
osteoarthropathy, fracture, thrombosis, venous stasis) 1 Mild
Local infection (as described above) with erythema >2 cm, or involving structures deeper than skin and
subcutaneous tissues (e.g., abscess, osteomyelitis, septic arthritis, fasciitis), and
No systemic inflammatory response signs (as described below)
Local infection (as described above) with the signs of SIRS, as manifested by two or more of the following: 3 Severea
Temperature >38C or <36C
Heart rate >90 beats/min
Respiratory rate >20 breaths/min or PaCO2 < 32 mm Hg
White blood cell count >12,000 or <4,000 cu/mm or 10% immature (band) forms 3
676 j
Table 6. A Comparison of contrasting debridement methods
Nonmechanical Selective and Specific for nonviable Tend to be slower (days to weeks) 1. Removal of potential source of infection 1. Contraindications will pertain to the
tissue and sepsis, primarily nonviable tissue. specific method of debridement (see
Convenient simple application 2. Removal of critically colonized tissue to below).
None or minimal discomfort decrease bacterial burden, reduce the 2. Refrain from debridement of dry and
Less costly probability of resistance from antibiotic intact eschars that have no clinical
treatment, and obtain accurate cultures. evidence of underlying infection and
3. Facilitate the collection of deep cultures could potentially serve as a biological
taken postdebridement to evaluate dressing.
requirements for antibiotic treatment
4. Stimulation of the wound bed to support
healing and prepare for procedures,
including but not limited to grafts, flaps,
and to support skin substitutes.
Autolytic Relies on a dressing type that Selective for nonviable tissue. Slow process (days to weeks) Same If there is active infection with large
permits the wound to remain None or minimal discomfort. May be associated with maceration of amounts of devitalized tissue needing
moist and facilitate autolysis Convenient simple application surrounding tissue. removal (i.e.) gangrenous tissue, a
of the devitalized tissue. Less costly Can be colonized and complicated by infection. different method of debridement
May be associated with maceration in should be considered.
surrounding tissue with highly exudative
wounds.
Not ideal in heavily infected wounds.
Less costly
Enzymatic Uses the application of an Quicker than Autolytic debridement Slow process (days to weeks) Same 1. A relative contraindication is its use in
enzyme, such as collagenase, Selective and specific for nonviable May be associated with maceration in heavily infected wounds.
to help lyse nonviable tissue. tissue. surrounding tissue with highly exudative 2. Collagenase should not be used with
None or minimal discomfort. wounds. silver-based products or with Dakin
Convenient simple application Not ideal in heavily infected wounds. solution.
May be deactivated by other treatments used in
wound care.
Expensive
Mechanical Relatively quicker than May be selective or nonselective depending on 1. Removal of potential source of infection 1. May vary depending on modality of
nonmechanical debridement specific method used. and sepsis, primarily necrotic tissue. mechanical debridement used (see
May be less convenient. 2. Removal of critically colonized tissue to below).
May be associated with more pain. decrease bacterial burden, reduce the 2. The presence of granulation tissue
Expensive probability of resistance from antibiotic covering the wound bed and the
treatment, and obtain accurate cultures. absence of devitalized tissue.
3. Facilitate the collection of deep cultures 3. Inadequate pain control.
taken postdebridement, to evaluate 4. Poor tissue perfusion and hypoxia
requirements for antibiotic treatment surrounding the anatomical region
4. Stimulation of the wound bed to support affected.
healing and prepare for future procedures, 5. Intact eschar with no gross clinical
including but not limited to grafts, flaps, evidence of an underlying infection
and to support skin substitutes. that could potentially serve as a
5. May require local or general anesthesia. biological dressing.
which is associated with inherent risk.
j
(continued)
677
678
j
Table 6. (Continued )
Sharp/surgical Uses a form of sharp instrument, Quick More postprocedure pain. Same 1. Operative debridement requires
such as a scalpel or scissor, Specific Expensive especially if requiring operative room appropriate surgical risk stratification
to mechanically remove Painful debridement. of the individual patient.
devitalized tissue in an Expensive 2. Patients with intact eschar and no
ambulatory or operative clinical evidence of an underlying
setting. infection should not be debrided when
the intact eschar functions as a
biological covering for the underlying
skin defect.
Wet to dry Utilizes saline-moistened gauze Quick Nonspecific nonselective removal of granulation Same Same as discussed in mechanical
that is allowed to dry and is Nonspecific tissue. debridement.
then removed with the Painful Postprocedure pain or discomfort.
nonselective mechanical May be associated with more cost
removal of devitalized tissue. as compared with some
nonmechanical debridement
methods.
Aqueous high-pressure Utilizes high-pressure irrigation, Quick Nonspecific Nonselective Same Same as discussed in mechanical
lavage irrigation, which can be done manually Suited for larger wounds. Less specific possibility of cross-contamination of debridement.
or whirlpool using a 20-mL syringe and an other wounds and infection. Risk of cross-contamination in the
18-gauge angiocatheter May be associated with postprocedure pain or presence of multiple wounds
delivering 12 psi or high- discomfort. May require immersion.
pressure jet stream of fluid Expensive
either from a whirlpool or
other mechanical irrigation
device.
Ultrasound debridement Utilizes a method of cavitation Quick May be associated with postprocedure pain of Same Contraindications: Same as discussed in
to generate sound energy Specific discomfort. mechanical debridement.
from a handheld instrument Risk of exposure to aerosolized organisms and
that through mechanical debris to the health care provider from the
means dislodges and removes wound.
devitalized tissue. Expensive
Biosurgery This method utilizes maggots Relatively quick May be associated with minor pain or Same 1. Abdominal wound contiguous with the
Maggot debridement that are applied in the larva Ultraspecific discomfort. intraperitoneal cavity.
therapy stage and consume Patient reluctance, psychological factors. 2. Pyoderma gangrenosum with
devitalized tissue selectively immunosuppression therapy.
and are removed usually 3. Wounds in close proximity to areas
within 3 days. afflicted by septic arthritis.
DEBRIDEMENT OF DIABETIC FOOT ULCERS 679
Gross dissection using instruments classi- vae).78 Medicinal maggots are believed to
fied as blunt are not capable of ultra- carry out biosurgical debridement of nonvi-
selective microdissection even in the hands able tissue selectively compared with blunt
of the most skilled health professionals. dissection, which may reduce the risk of
Microdissection may only be possible with secondary superinfection.78–81
the use of biosurgery or maggot debride- The maggots are capable of consuming bac-
ment therapy (MDT) described separate- teria and are believed to produce antimicro-
ly.75 This approach may be problematic in bial secretions.75 This has been demonstrated
that every ‘‘new’’ injury increases the risk of through mechanistic in vitro studies.79 MDT
complicating superinfection.9,59,60 may have antimicrobial properties that are
(2) Wet to dry mechanical debridement removes active against hospital acquired resistant or-
nonviable tissue by allowing gauze satu- ganisms, such as MRSA.79 They may secrete
rated with saline and applied to a wound, substances that stimulate wound healing.79
to dry. The gauze then becomes adherent
to the wound during the drying phase and
when the gauze is removed it can non- STANDARD WOUND CARE,
selectively pull away both nonviable tissue AND ADJUNCTIVE PREVENTION,
along with viable granulation tissue.3,75 AND TREATMENT METHODS
(3) Aqueous high-pressure lavage/irrigation The treatment of a DFU generally involves a
involves a jet stream of saline/water that multidisciplinary team approach and includes com-
mechanically removes nonviable tissue.75 prehensive advanced wound care. This team may
This is considered a nonselective form of comprise a primary care physician, a wound care
debridement and is capable of removing physician, a wound care nurse, a nutritionist, or-
granulation tissue and may pose a risk to thotics consultant, physical therapist, and a hy-
the health care provider.75 The mist created perbaracist.3,48 This comprehensive advanced
by the high-pressure irrigation may expose wound care approach is endorsed through ad-
the provider to contamination.3,75 Whirlpool vocacy by the Alliance of Wound Care Stake-
involves a form of high-pressure hydro irri- holders involving a multidisciplinary team and
gation where the entire limb or patient is the following interventions.3,48
immersed in a whirlpool bath during the (1) Off-loading: Weight-bearing redistribution is
irrigation process.48 the most important consideration for wound
Cross-contamination is possible using this healing of the DFU. This provides support by
method as other wounds and body surfaces redistribution of weight bearing away from
may be immersed in the same aqueous so- the wound and relocates it to the adjacent
lution.48 This is also considered a nonselec- surfaces of the affected foot or leg through the
tive form of debridement.3,75 use of orthotics. A common error in wound care
(4) Ultrasound debridement utilizes sound en- includes neglecting this critical intervention.
ergy to mechanically debride wounds through Since sensory neuropathy perpetuates a vi-
contact or noncontact low-frequency ultra- cious cycle of reinjury due to unrecognized
sound energy.75,76The process utilizes a trauma, offloading becomes critical in break-
method of cavitation to generate sound en- ing this self-perpetuating cycle.82–84
ergy from a hand-held instrument, which Alternatively, complete offloading can be achi-
through mechanical means dislodges and eved by using wheelchairs, walkers, crutches,
removes devitalized tissue. Contamination or other wheeled mobile devices to remove
to the operator/provider can also occur due all weight-bearing entirely (nonweight
to aerosolization. bearing) from the affected wound and limb.3
(5) Biosurgery or MDT—This has been an area (2) Physical therapy: The use of offloading
of interest for over 400 years and provides a equipment may require special instruction
complex system of wound care.75 Maggots routinely provided by a physical therapy
are larva of flies, such as Lucilia Sericata department in the proper use of crutches,
that consume nonviable tissue selectively.77 wheelchair, or other ancillary mobile
This is typically done in the United States nonweight-bearing equipment.
with another form of larva, the blow The patient may require rehabilitation due
fly maggot variety (Phoenicia sericata lar- to long periods of immobility to regain
680 DAYYA ET AL.
function and strength to allow for the use of of hyperbaric oxygen therapy through pe-
offloading devices this can be done through ripheral vasoconstriction without a negative
intensive short-term inpatient rehabilita- effect on tissue oxygenation. Oxygen diffusion
tion or in an outpatient or home setting. is increased up to a factor of four in the af-
(3) Medical optimization of comorbidities, in- fected tissues.86 Antimicrobial tissue pene-
cluding diabetes: The patient requires med- tration and leukocyte function is believed to be
ical optimization of current treatment for enhanced by the use of hyperbaric oxygen
diabetes and other conditions that if left therapy. Susceptible organisms, such as an-
untreated or poorly controlled may impede aerobic or facultative anaerobic organisms
wound healing. that do not tolerate high oxygen tensions may
(4) Nutritional consultation services and supple- be inhibited by using hyperbaric oxygen
mentation: These services have been uti- therapy. An increase in stem cell production,
lized to address nutritional deficiency states differentiation, and presence in the wound
that may impede wound healing. Labora- bed has been demonstrated.87 Hyperbaric ox-
tory markers, such as Total Lymphocyte ygen therapy may be especially useful in those
Count, pre-Albumin, Albumin, and Total diabetics that have had wound care for greater
Protein, along with clinical parameters than 4 weeks with poor or no response to ad-
have been used to help direct nutritional vanced wound care treatment.3,88
interventions. The use of supplementation
Topical oxygen involves delivering oxygen
including protein supplements and micro-
over and in contact with the wound site rather
nutrients may be warranted.
than through the systemic circulation as de-
(5) Infection eradication: If the wound is criti- livered through Hyperbaric oxygen therapy.
cally colonized or infected then this may Studies using topical oxygen delivery have
impair wound healing and antimicrobial been reviewed in a position statement by the
therapy is often prescribed. Treatment can Undersea and Hyperbaric Medical Society in
be directed locally or systemically depending 2005 and revised in 2018. To date, there is
on the extent and severity of the infection. insufficient evidence to conclude that topical
(6) Medical and surgical vascular interventions: delivery of oxygen should be used in lieu of
Hemodynamically significant macrovascular systemic hyperbaric oxygen delivery.89
insufficiency can compound microarterial (8) Coordination of care: This comprehensive
insufficiency and may require vascular sur- approach includes communication between
gery evaluation. Therapy may involve more the advanced specialties for wound care (e.g.,
extensive medical treatment, and/or the pa- surgeons, toe and flow teams, specialized
tient may require surgical revascularization, DFU centers) with the respective primary
which could include angioplasty, stenting, care physicians and home health providers
atherectomy, or surgical bypass grafting. who are involved in medical optimization of
(7) Hyperbaric oxygen therapy and other means the patient’s health conditions, including di-
of oxygen delivery: Periwound tissue hypoxia abetes. The accessibility in rural areas may
can be measured using transcutaneous oxi- be complicated. Telemedicine has afforded
metry. If tissue hypoxia is found to be revers- the opportunity to offset the limitation in
ible with normobaric or hyperbaric oxygen rural regions for access to wound care pro-
challenge, then hyperbaric oxygen therapy fessionals. Wound care professionals re-
has been considered adjuvant therapy in motely may have visual oversight that is
healing problem refractory wounds in diabet- facilitated through the work of an onsite
ics. This testing may reveal microvascular wound care nurse or other health care pro-
insufficiency. Hyperbaric oxygen therapy may fessional. Disease progression can result due
increase tissue oxygen tensions up to 15 times to incomplete information sharing between
normal. Angiogenesis and vasculogenesis the members of the multidisciplinary team,
may be stimulated by the using hyperbaric lost follow-ups, and patient noncompliance.
oxygen therapy, which may enhance the blood The importance of intensive and close follow-
supply around the wound. Proinflammatory up, including regular podiatric care, de-
intracellular adhesion molecules are down- bridement, access to vascular in-hospital
regulated providing an anti-inflammatory ef- intervention to maximize the likelihood of
fect.85 Edema may be decreased with the use limb salvage, is critical.90
DEBRIDEMENT OF DIABETIC FOOT ULCERS 681
Work-Flow Diagram: Considerations for the Treatment and Management of the Diabetic
Foot Ulcer
Evaluation for Osteomyelitis consider: CT, MRI, Bone Scan, or bone debridement,
biopsy/pathology.
Consider other advanced wound therapies (wound vacuum therapy, skin substitutes,
collagen matrix, growth factors)
REFERENCES
1. International Working Group on the Diabetic 11. Tennvall GR, Apelqvist J, Eneroth M. Costs 23. Barnes JA, Eid MA, Creager MA, Goodney PP. Epi-
Foot. IWGDF Guidelines on the prevention and of deep foot infections in patients with diabetes demiology and risk of amputation in patients with
management of diabetic foot disease. Maas- mellitus. Pharmacoeconomics 2000;18:225–238. diabetes mellitus and peripheral artery disease.
tricht, The Netherlands: International Working Arterioscler Thromb Vasc Biol 2020;40:1808–1817.
12. Cosgrove MP, Sargeant LA, Caleyachetty R,
Group on the Diabetic Foot, 2019.
Griffin SJ. Work-related stress and Type 2 dia- 24. National Institute of Diabetic and Digestive and
2. Sumpio BE. Foot ulcers. N Engl J Med 2000;343: betes: systematic review and meta-analysis. Kidney Diseases. Washington, DC: National
787–793. Occup Med (Lond) 2012;62:167–173. Diabetes Statistics Report. 2020.
3. Sheffield PJ, Fife CE, Smith AP. Wound Care 13. Kumari M, Head J, Marmot M. Prospective study 25. Ashry HR, Lavery LA, Armstrong DG, Lavery DC,
Practice. Flagstaff, AZ: Best Publising Company, of social and other risk factors for incidence of van Houtum WH. Cost of diabetes-related am-
2004. type 2 diabetes in the Whitehall II study. Arch putations in minorities. J Foot Ankle Surg 1998;
Intern Med 2004;164:1873–1880. 37:186–190.
4. Margolis DJ, Allen-Taylor L, Hoffstad O, Berlin
JA. Diabetic neuropathic foot ulcers: the asso- 14. Nakata A. Psychosocial job stress and immunity: 26. Association AD. Diabetes Statistics. Arlington,
ciation of wound size, wound duration, and a systematic review. Methods Mol Biol 2012; VA: American Diabetes Association, National
wound grade on healing. Diabetes Care 2002;25: 934:39–75. Diabetes Fact Sheet. 2011.
1835–1839.
15. USDC. US Agency for Healthcare Quality and
27. Robbins JM, Strauss G, Aron D, Long J, Kuba J,
5. Diabetes.org.uk. Diabetes Reports and Statistics Research. Washington, DC: National Healthcare
Kaplan Y. Mortality rates and diabetic foot ul-
2019. Diabetes.org.uk, 2019. Quality Report 2011. 2012.
cers: is it time to communicate mortality risk to
6. National Institute of Health Diabetic Foot Con- 16. Ramsey SD, Newton K, Blough D, et al. Incidence, patients with diabetic foot ulceration? J Am
sortium. Diabetic Foot Consortium 2020. http:// outcomes, and cost of foot ulcers in patients with Podiatr Med Assoc 2008;98:489–493.
diabeticfootconsortium.org/ (last accessed April diabetes. Diabetes Care 1999;22:382–387.
1, 2021). 28. Tentolouris N, Al-Sabbagh S, Walker MG,
17. Boulton AJM AD, Kirsner RS, Attinger CE, et al. Boulton AJ, Jude EB. Mortality in diabetic and
7. Centers for Disease Control and Prevention. Diagnosis and Management of Diabetic Foot nondiabetic patients after amputations per-
National diabetes fact sheet: national estima- Complictions. Arlington, VA: American Diabetes formed from 1990 to 1995: a 5-year follow-up
tes and general information on diabetes and Association, 2018. study. Diabetes Care 2004;27:1598–1604.
prediabetes in the United States. Atlanta, GA:
18. Zhang P, Lu J, Jing Y, Tang S, Zhu D, Bi Y. 29. Diabetes UK. Facts and Stats. London, England:
Centers for Disease Control and Prevention,
Global epidemiology of diabetic foot ulceration: Diabetes UK, 2015.
2012.
a systematic review and meta-analysis. Ann
8. Steed DL, Donohoe D, Webster M, Lindsley L, Med 2017;49:106–116. 30. Yazdanpanah L, Nasiri M, Adarvishi S. Literature
Group PS. Extensive debridement of human di- review on the management of diabetic foot ul-
19. Consensus Development Conference on Diabetic cer. World J Diabetes 2015;6:37–53.
abetic foot ulcers is a vital adjunct to healing.
Foot Wound Care: 7–8 April 1999, Boston,
5th Annual Meeting of the European Tissue
Massachusetts. American Diabetes Association. 31. National Institute for Health and Care Ex-
Repair Society; August 30–September 2, 1996;
Diabetes Care 1999;22:1354–1360. cellence. Diabetic Foot Problems: Prevention and
Padova, Italy, 1996:371.
Management. London, United Kingdom: National
20. Friel K. Componentry for lower extremity prosthe-
9. Bakker K, Schaper NC, International Working Institute for Health and Care Excellence, 2016.
ses. J Am Acad Orthop Surg 2005;13:326–335.
Group on Diabetic Foot Editorial B. The devel-
32. National Amputee Statistical Database. The
opment of global consensus guidelines on the 21. Dillingham TR, Pezzin LE, MacKenzie EJ. Limb
Amputee Statistical Database for the United
management and prevention of the diabetic foot amputation and limb deficiency: epidemiology
Kingdom. In: Information Service Division NHS
2011. Diabetes Metab Res Rev 2012;28 Suppl 1: and recent trends in the United States. South
Scotland, ed. Edinburgh, 2005.
116–118. Med J 2002;95:875–883.
33. Network. SIG. Management of Diabetic Foot
10. International Working Group of the Diabetic 22. Sugarman JR, Reiber GE, Baumgardner G, Prela CM, Disease. Implementation of the St. Vincent De-
Foot. Diabetic Foot—Epidemiology, Psychoso- Lowery J. Use of the therapeutic footwear benefit claration. The Care of Patients in Scotland 1997.
cial, and Economic Factors. Maastricht, The among diabetic medicare beneficiaries in three Edinburgh, Scotland: Scottish Intercollegiate
Netherlands: IWGoD, 2012. states, 1995. Diabetes Care 1998;21:777–781. Guidelines, 1997.
DEBRIDEMENT OF DIABETIC FOOT ULCERS 685
34. Scottish Intercollegiate Guidelines Network 51. Abbott RD, Brand FN, Kannel WB. Epidemiology of 67. Cutting K. Glossary. In: Miller M, Glover G, eds.
(SIGN). Search filters. 2009. http://www.sign some peripheral arterial findings in diabetic men Wound Management: Theory and Practice (Chap-
.ac.uk/methodology/filters.html#random (last ac- and women: experiences from the Framingham ter 7). London: Johnson & Johnson Medical Ltd,
cessed May 21, 2016). Study. Am J Med 1990;88:376–381. 1999:170–173.
35. Spencer S. Pressure relieving interventions for 52. Research Boston Medical Center Stroke and 68. Szablewski L, Sulima A. The structural and
preventing and treating diabetic foot ulcers. Cerebral Vascular CenterReseacrh. U.S Public functional changes of blood cells and molecular
Cochrane Database Syst Rev 2000:CD002302. Health Service - Framingham Study 2021. https:// components in diabetes mellitus. Biol Chem
www.bmc.org/stroke-and-cerebrovascular-center/ 2017;398:411–423.
36. WHO. NCD Country Profiles—UK. Geneva,
research/framingham-study (last accessed Jan-
Switzerland: World Health Organization, 2016. 69. Armstrong DG, Boulton AJM, Bus S. Diabetic
uary 2, 2021).
foot ulcers and their recurrence. N Engl J Med
37. Calman K. On the state of the public health. The
53. Pecoraro RE, Reiber GE, Burgess EM. Pathways 2017;376:2367–2375.
Annual Report of the Chief Medical Officer of
to diabetic limb amputation. Basis for preven-
the Department of Health for the Year 1997. 70. Fw W. A classification and treatment program
tion. Diabetes Care 1990;13:513–521.
Washington, DC: The Stationery Office, 1998. for diabetic, neuropathic, and dysvascular foot
54. Reiber GE, Vileikyte L, Boyko EJ, et al. Causal problems. American Academy of Orthopedic
38. International Diabetes Federation. The Interna- pathways for incident lower-extremity ulcers in Surgery 1979;27:143–165.
tional Diabtes Federation (IDF) Consensus
patients with diabetes from two settings. Dia-
Worldwide Definition of the Metabolic Syn- 71. Fw W. The dysvascular foot: a system for diag-
betes Care 1999;22:157–162.
drome. Washington, DC: International Diabetes nosis and treatment. Foot Ankle 1981;2:64–122.
Federation, 2006. 55. Siitonen OI, Niskanen LK, Laakso M, Siitonen JT,
72. Lavery LA, Armstrong DG, Harkless LB. Classifi-
Pyorala K. Lower-extremity amputations in dia-
39. Bommer C, Sagalova V, Heeseman E, et al. cation of diabetic foot wounds. J Foot Ankle
betic and nondiabetic patients. A population-
Global economic burden of diabetes in adults: Surg 1996;35:528–531.
based study in eastern Finland. Diabetes Care
projections from 2015 to 2030. Diabetes Care 1993;16:16–20. 73. Oyibo SO, Jude EB, Tarawneh I, Nguyen HC,
2018;41:963–970. Harkless LB, Boulton AJ. A comparison of two
56. Boulton A. The pathway to ulceration: aetio-
40. Dall TM, Yang W, Halder P, et al. The economic diabetic foot ulcer classification systems: the
pathogenesis. In: Boulton A, Connor H, Cavanagh
burden of elevated blood glucose levels in 2012: Wagner and the University of Texas wound clas-
PR, eds. The Foot in Diabetes, 3rd ed. Chiche-
diagnosed and undiagnosed diabetes, gesta- sification systems. Diabetes Care 2001;24:84–88.
ster: John Wiley & Sons Ltd, 2000:19–31.
tional diabetes mellitus, and prediabetes. Dia- 74. Mills JL, Conte MS, Armstrong DG, Sidawy AN,
betes Care 2014;37:3172–3179. 57. Panayiotopoulos YP, Tyrrell MR, Arnold FJ,
Andros G. The Society for Vascular Surgery lower
Korzon-Burakowska A, Amiel SA, Taylor PR.
41. American Diabetes Association. Statistics - The extremity threatened limb classification system:
Results and cost analysis of distal [crural/pedal]
Cost of Diabetes. March 22, 2018. Report No. risk stratification based on Wound, Ischemia, and
arterial revascularisation for limb salvage in di-
foot Infection (WIfI). J Vasc Surg 2014;59:220–234.
42. Holzer SE, Camerota A, Martens L, Cuerdon T, abetic and non-diabetic patients. Diabet Med
Crystal-Peters J, Zagari M. Costs and duration of 1997;14:214–220. 75. Strohal R, Apelqvist J. EWMA Document: de-
care for lower extremity ulcers in patients with bridement: an updated overview and clarification
58. Neuman TS, Thom SR. Physiology and Medicine
diabetes. Clin Ther 1998;20:169–181. of the principle role of debridement. J Wound
of Hyperbaric Oxygen Therapy. North Beach, FL:
Care 2013;22:S1–S49.
43. National Center for Health Statistics. Health, Saunders, 2008.
United States, 2009, with chart book on trends in 76. Campitiello F, Mancone M, Della Corte A,
59. Edwards J, Stapley S. Debridement of diabetic
the health of Americans. In: Health, editor. Wa- Guerniero R, Canonico S. An evaluation of an
foot ulcers. Cochrane Database Syst Rev 2010:
shington, DC: U.S Government Printing Office, 2010. ultrasonic debridement system in patients with
CD003556.
diabetic foot ulcers: a case series. J Wound Care
44. CDC. CDC Diabetes Report Card. In: Services 60. Smith J. Debridement of diabetic foot ulcers. 2018;27:222–228.
UDoHaH, ed. Arlington, VA: Centers for Disease Cochrane Database Syst Rev 2002:CD003556.
Control Prevention, 2017. 77. Chan DC, Fong DH, Leung JY, Patil NG, Leung GK.
61. Atkin L, Tansley J, Stephenson J. Diabetic foot Maggot debridement therapy in chronic wound
45. Harrington C, Zagari MJ, Corea J, Klitenic J. A ulceration: the impact of edema. Wounds UK care. Hong Kong Med J 2007;13:382–386.
cost analysis of diabetic lower-extremity ulcers. 2018;14:33–39.
Diabetes Care 2000;23:1333–1338. 78. Pettican A, Baptista C. Maggot debridement
62. Faris I, Parkhouse N, Quesne PL. The Manage- therapy and its role in chronic wound manage-
46. Marks L. Counting the Cost: The Real Impact of ment of the Diabetic Foot, 2nd ed. Edinburgh: ment. Singapore Nurs J 2012;39:27–33.
Non-Insulin-Dependent Diabetes. Fund KS, Dia- New York: Churchill Livingstone, 1991:41–64.
betic AB, eds. London, England: King’s Fund 79. Margolin L, Gialanella P. Assessment of the
Policy Unit, 1996. 63. Orasanu G, Plutzky J. The continuum of diabetic antimicrobial properties of maggots. Int Wound
vascular disease: from macro- to micro. J Am J 2010;7:202–204.
47. NHS. NHS Diabetes calls for specialist diabetic Coll Cardiol 2009;53:S35–S42.
foot care teams to save limbs, lives and millions 80. Tian X, Liang XM, Song GM, Zhao Y, Yang XL.
for the NHS. London, England: National Health 64. Bus SA, Yang QX, Wang JH, Smith MB, Maggot debridement therapy for the treat-
Service, 2012. Wunderlich R, Cavanagh PR. Intrinsic muscle ment of diabetic foot ulcers: a meta-analysis.
atrophy and toe deformity in the diabetic neu- J Wound Care 2013;22:462–469.
48. Baronski S, Ayello EA. Wound Care Essentials ropathic foot: a magnetic resonance imaging
Principles and Practice. Wilkins LW, ed. Phila- 81. Steenvoorde P, Jacobi CE, Van Doorn L, Oskam
study. Diabetes Care 2002;25:1444–1450.
delphia: Wolters Kluwer, 2008. J. Maggot debridement therapy of infected ul-
65. Faris I. Mechanisms for the development of foot cers: patient and wound factors influencing
49. Myers BA. Wound Management Principles and lesions. In: Faris I, ed. The Management of the outcome—a study on 101 patients with 117
Practice. Upper Saddle River: Pearson, Prentice Diabetic Foot, 2nd ed. Edinburgh: Churchill wounds. Ann R Coll Surg Engl 2007;89:596–602.
Hall, 2008. Livingstone, 1991:5–9.
82. Braun LR, Fisk WA, Lev-Tov H, Kirsner RS,
50. Faris I. Vascular disease. In: Faris I, ed. The 66. Edmonds M, Foster A. Stage 3: the ulcerated Isseroff RR. Diabetic foot ulcer: an evidence-
Management of the Diabetic Foot. 2nd ed. foot. In: Managing the Diabetic Foot. Hoboken, based treatment update. Am J Clin Dermatol
Edinburgh: Churchill Livingstone, 1991:9–40. NJ: Wiley Blackwell, 2000:45–76. 2014;15:267–281.
686 DAYYA ET AL.
83. Bus SA, Armstrong DG, Gooday C, et al. Guide- 92. Royal College of General Practitioners, British foot wounds in people with diabetes mellitus.
lines on offloading foot ulcers in persons with Diabetic Association, Royal College of Physi- Cochrane Database Syst Rev 2013:CD010318.
diabetes (IWGDF 2019 update). Diabetes Metab cians, Royal College of Nursing (collaborative
101. Voigt J, Wendelken M, Driver V, Alvarez OM.
Res Rev 2020;36 Suppl 1:e3274. programme). Prevention and Management of
Low-frequency ultrasound (20–40kHz) as an
Foot Problems. Clinical Guidelines for Type 2
84. Wilcox JR, Carter MJ, Covington S. Frequency of adjunctive therapy for chronic wound healing:
Diabetes. London, England: Royal College of
debridements and time to heal: a retrospective a systematic review of the literature and
General Practitioners, 2000.
cohort study of 312 744 wounds. JAMA Der- meta-analysis of eight randomized controlled
matol 2013;149:1050–1058. 93. Margolis DJ, Kantor J, Berlin JA. Healing of trials. Int J Low Extrem Wounds 2011;10:190–
diabetic neuropathic foot ulcers receiving stan- 199.
85. Thom SR. Hyperbaric oxygen therapy. J Intensive
dard treatment. A meta-analysis. Diabetes Care
Care Med 1989;4:58–74.
1999;22:692–695.
86. Fife CE, Buyukcakir C, Otto G, Sheffield P, Love T,
94. Mason J, O’Keeffe C, Hutchinson A, McIntosh A,
Warriner R, 3rd. Factors influencing the outcome Abbreviations and Acronyms
Young R, Booth A. A systematic review of
of lower-extremity diabetic ulcers treated with
foot ulcer in patients with type 2 diabetes mel- ABI ¼ ankle-brachial index
hyperbaric oxygen therapy. Wound Repair Regen
litus. II: treatment. Diabet Med 1999;16:889–909. DFU ¼ diabetic foot ulcer(s)
2007;15:322–331.
DM ¼ diabetes mellitus
95. Game FL, Hinchliffe RJ, Apelqvist J, et al. A sys-
87. Thom SR, Bhopale VM, Velazquez OC, Goldstein IDF ¼ International Diabetes
tematic review of interventions to enhance the
LJ, Thom LH, Buerk DG. Stem cell mobilization by Federation
healing of chronic ulcers of the foot in diabetes.
hyperbaric oxygen. Am J Physiol Heart Circ IWGDF ¼ International Working Group
Diabetes Metab Res Rev 2012;28 Suppl 1:119–141.
Physiol 2006;290:H1378–H1386. on the Diabetic Foot
96. Hinchliffe RJ, Valk GD, Apelqvist J, et al. A MDT ¼ biosurgery or maggot debridement
88. UMHS. Hyperbaric Oxygen Therapy Indications:
systematic review of the effectiveness of inter- therapy
The Hyperbaric Oxygen Therapy Committee Re-
ventions to enhance the healing of chronic ulcers MRA ¼ magnetic resonance angiogram
port. North Beach, FL: Undersea and Hyperbaric
of the foot in diabetes. Diabetes Metab Res Rev MRSA ¼ methicillin-resistant Staphylococcus
Medical Society, 2008, 0930406230.
2008;24 Suppl 1:S119–S144. aureus
89. Feldmeier JJ, Hopf HW, Warriner RA III, Fife CE, NHS ¼ National Health Service
97. Dumville JC, Deshpande S, O’Meara S, Speak K.
Gesell LB, Bennett M. UHMS position statement: PAD ¼ peripheral arterial disease
Hydrocolloid dressings for healing diabetic foot
topical oxygen for chronic wounds. Undersea PVR ¼ pulse volume recording
ulcers. Cochrane Database Syst Rev 2012:
Hyperb Med 2005;32:157–168. SPP ¼ skin perfusion pressure
CD009099.
SR ¼ systematic review
90. Montero-Baker M, Zulbaran-Rojas A, Chung J,
98. Dumville JC, O’Meara S, Deshpande S, Speak K. TcPO2 ¼ transcutaneous partial pressure
et al. Endovascular therapy in an ‘‘all-comers’’
Alginate dressings for healing diabetic foot of oxygen/transcutaneous
risk group for chronic limb-threatening is-
ulcers. Cochrane Database Syst Rev 2013: oximetry
chemia demonstrates safety and efficacy
CD009110. TMA ¼ transmetatarsal amputation
when compared with the established perfor-
TP ¼ toe pressure
mance criteria proposed by the society for 99. Dumville JC, Deshpande S, O’Meara S, Speak K.
Wifi ¼ wound, ischemia, foot infection
vascular surgery. Ann Vasc Surg 2020;67:425– Foam dressings for healing diabetic foot ulcers.
(Society of Vascular Surgery
436. Cochrane Database Syst Rev 2011:CD009111.
threatened limb ischemia
91. Dorland’s Electronic Medical Dictionary. Dorland: 100. Dumville JC, Hinchliffe RJ, Cullum N, et al. classification system.)
W.B. Saunders Company, 1998. Negative pressure wound therapy for treating