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Pressure ulcers: A critical review of definitions and classifications

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FEATURE

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Pressure Ulcers: A Critical Review of
Definitions and Classifications

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Jan Kottner, RN, PhD; Katrin Balzer, RN, MA; Theo Dassen, RN, PhD; and Sarah Heinze, MD, PhD

Abstract

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Pressure ulcers are serious health problems. Although a vast amount of literature addresses prevention and treatment
strategies, conceptual difficulties persist regarding pressure ulcer definitions, classifications, and distinction from other
tissue lesions. Based on a review of terminologies as well as current state of knowledge on pathophysiology and etiology,
questions as to what pressure ulcers are and what they are not are addressed. Because pressure forces seem to play a
minor role in the development of superficial ulcers, the authors suggest these types of wounds no longer be termed pres-
sure ulcers. A more general term such as decubitus ulcer may be a more appropriate way to characterize wounds that
emerge as a result of compressive forces, shearing forces, and/or friction in patients dependent on skilled care. For clinical
practice, a two-category classification is proposed: superficial ulcers predominantly caused by friction and deep ulcers

PR
predominantly caused by pressure. This simple classification could enhance diagnostic accuracy and reliability. Multidis-
ciplinary communication and research is needed to develop valid and reliable definitions and classifications for pressure
ulcer-like wounds.

Key Words: pressure ulcers, definitions, concepts, diagnosis, validity

Index: Ostomy Wound Management 2009;55(9):22–29

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Potential Conflicts of Interest: none disclosed

ressure ulcers are common and their development is com- and PubMed. Terms such as bedsore or decubitus are synonym
P plex. Even though terms to describe these wounds and the
systems to classify them have undergone numerous revisions,
entry terms that refer to the medical subject heading (MeSH)
pressure ulcer that was not introduced until 2006. The Library
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there are still conceptual difficulties. It is important to clarify of Medicine7 describes a pressure ulcer as “an ulceration
the concept of pressure ulcers to ensure accurate diagnosis, caused by prolonged pressure on the skin and tissues when
communication, prevention, and treatment decisions. The one stays in one position for a long period of time, such as
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purpose of this review is to examine commonly used pressure
ulcer definitions and classifications and to propose a simple
solution to overcome diagnostic problems and uncertainty in
clinical practice.
What are Pressure Ulcers?
The term pressure ulcer became popular in the early
1970s.1,2 Previous terms for skin and tissue lesions of this type
included bedsores3,4 or decubitus ulcers.5,6 Use of the newer term
is reflected in the US National Library of Medicine’s con-
DO
lying in bed. The bony areas of the body are the most fre-
quently affected sites which become ischemic under sustained
and constant pressure.”
The Excerpta Medica database (EMBASE) produced by El-
sevier uses terms such as pressure ulcer, bedsore, or pressure sore
synonymously as key words referring to the subject heading
decubitus, introduced in 1979. In EMBASE, decubitus belongs
to the category skin ulcers. Similarly, in the International Sta-
tistical Classification of Diseases and Related Heath Problems
(ICD-10), the term pressure ulcer refers to the diagnosis decu-

trolled vocabulary used for indexing articles for MEDLINE bitus ulcer (L89), which also belongs to the category diseases

Dr. Kottner is an assistant professor, Centre for Humanities and Health Sciences, Department of Nursing Science, Charite-Universitätsmedizin Berlin, Germany.
Ms. Balzer is an assistant professor, Nursing Research Group, Institute for Social Medicine, Universitätsklinikum Schleswig-Holstein, Lübeck, Germany. Dr. Dassen
is Institute Director, Centre for Humanities and Health Sciences, Department of Nursing Science, Charite-Universitätsmedizin Berlin. Dr. Heinze is a senior physician,
Institute of Legal Medicine and Forensic Sciences, Charite-Universitätsmedizin. Please address correspondence to: Jan Kottner, RN, PhD, Department of Nursing
Science, Charite-Universitätsmedizin Berlin, Augusteneburger Platz 1, 13353 Berlin, Germany; email: jan.kottner@charite.de.

22 OSTOMY WOUND MANAGEMENT SEPTEMBER 2009 www.o-wm.com

 PRESSURE ULCERS AND THEIR CLASSIFICATION
of the skin and subcutaneous tissue.8 Further explanations or
definitions are not given.
Two more detailed definitions that have been widely
adopted in clinical practice and research were provided by the
European Pressure Ulcer Advisory Panel (EPUAP) and the
National Pressure Ulcer Advisory Panel (NPUAP). The
EPUAP9 defines a pressure ulcer as “...an area of localised
damage to the skin and underlying tissue caused by pressure,
shear, friction, and/or a combination of these.” According to
the NPUAP,10 a pressure ulcer is “...localized injury to the skin
and/or underlying tissue usually over a bony prominence, as
a result of pressure, or pressure in combination with shear
and/or friction.”
According to the presented definitions, the factor pressure
seems to play a key role in pressure ulcer development;
whereas, the factors shear and friction are included only in the
EPUAP and NPUAP definitions.
Pressure. The relationship between long-enduring pres-
PR
sure and tissue damage is well established.6,11,12 In the sitting
or lying position, tissue is compressed between the underlying
surface and bony prominences, which explains why most pres-
sure ulcers are located at these body sites. However, the process
of tissue breakdown is not yet fully understood. Reviews of
the literature13,14 consolidate pressure ulcer causation into four
main theories:
1. Ischemia caused by capillary occlusion. Applied pressure
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causes capillary occlusion, leading to ischemia. Cellular
metabolism is interrupted and metabolic waste products
are accumulated; these actions change capillary perme-
ability, leading to edema and cellular infiltration. In-
creasing the degree and duration of ischemia not only
increases changes in membrane permeability and ex-
travasation, but also enhances cellular necrosis and in-
flammatory reactions.6,15
2. Reperfusion injury. During the ischemic period, affected
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tissue reduces metabolism in order to reduce hypoxic
and ischemic damage and to preserve tissue function.
When reperfusion occurs, liberated free radicals cause
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inflammatory responses and advance cell damage.16-19
3. Lymphatic function is impaired. Pressure reduces the
blood supply, which leads to hypoxia. Hypoxia damages
the lymphatic vessels; subsequently, lymphatic motility
is lost and lymph flow impaired. Metabolic waste prod-
ucts are accumulated, leading to tissue necrosis.20 Small
amounts of pressure seem to increase the lymphatic
drainage but when a critical point is exceeded, lymph
flow is reduced.21
4. Mechanical deformation of tissue cells. Pressure leads to
DO
large deformation of tissue and cells, consequently trig-
gering volume changes and cytoskeletal reorganization
that cause initial damage and tissue breakdown.22-24 Cell
membrane rupture due to cell-to-cell contact also was
considered to cause irreversible tissue damage.20
Regardless of the relevance of these individual theories, it
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Ostomy Wound Management 2009;55(9):22–29
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Key Points
• The continuing dilemma of what to call pressure ul-
cers and ever-changing classification definitions ham-
per progress in their prevention and care.
• The authors critically review commonly used terms
and provide suggestions to overcome diagnostic
problems and uncertainty in clinical practice.
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is highly probable that all four processes contribute to pressure
ulcer formation.14,22 However, pressure-induced tissue damage
is related not only to body sites, but also to the type of tissue in-
volved. Muscle and/or subcutaneous fat have been found to be
more sensitive to compression than skin and fascia.11,14,16,25-27
The skin (epidermis and dermis) survives longer periods of
ischemia without irreversible damage as compared to muscle
tissue.28 Therefore, pressure-induced tissue injuries always
start in the muscle and/or subcutaneous fat; visible skin dam-
age occurs later.11,14,16,17,19,26-28
Shear. Shear distorts and compresses tissue. Pressure is
thought to have a perpendicular effect on tissue; shear exerts
diagonal force. However, a firm distinction between pressure
and shear is hardly possible because pressure always causes
shear and shear causes compressive forces within the strained
tissue.12,17,29 Comparable to pressure forces, deeper structures
like muscle and subcutaneous fat are more sensitive and vul-
nerable than the skin to shear25 because the skin contains col-
lagen and elastic fibers that provide tensile strength.
Friction. Friction inflicts parallel forces on the skin, found
to be especially damaging to superficial layers.25,26,30 Additional
factors (eg, moisture due to incontinence) also contribute to
the development of superficial skin lesions. However, although
the skin can become macerated and inflamed, neither friction
nor moisture has been found to lead to deeper tissue layer
damage,14,17,31 an observation recently supported by high-res-
olution ultrasound scans that show that while friction affects
the dermis, deep tissue layers remain intact.32,33
In summary, according to current pathogenetic knowledge,
both compressive and shearing forces seem to primarily affect
deeper tissue layers; whereas, friction appears to solely contribute
to superficial lesions. Taking these different etiological mecha-
nisms into account, the term pressure ulcer, as defined to date,
covers a broad range of types of wounds, but not all of them are
necessarily caused by pressure or shear. Therefore, the question
remains: Are all pressure ulcers actually pressure ulcers?
How are Pressure Ulcers Classified?
Pressure ulcers are classified according to their visible clin-
ical appearance. The first well-documented pressure classifi-
cation system was proposed by Shea in 1975.34 Shea
differentiated five categories: the category “Closed Pressure
Sore,” indicating deep tissue injury under intact skin, and
grades 1 to 4 where increasing numbers indicate more severe
SEPTEMBER 2009 OSTOMY WOUND MANAGEMENT 23
FEATURE
tissue damage. In subsequent years, this classification was
modified several times and new classification systems with
varying numbers of categories have been introduced. Most
classifications demonstrate increasing numbers of grades or
stages to indicate more extensive damage to deeper tissue lay-
ers. However, there are glaring distinctions among the defini-
tions and the number of categories comprising the two most
popular classifications (EPUAP and NPUAP) (see Table 1).
This causes serious problems for international communica-
tion and research — issues that are being addressed by a joint
NPUAP/EPUAP initiative.
The degree of reliability of these classifications is contra-
dictory. At present, no empirical evidence recommending a
specific pressure ulcer classification system for use in daily
practice has been found.35 In general, it seems that practition-
ers most often disagree regarding 1) the diagnosis of non-
blanchable erythema (grade 1/Stage I pressure ulcers) and 2)
the differentiation between superficial pressure ulcers (grade 2
PR
/Stage II pressure ulcers) and moisture-related skin lesions.36-39
Furthermore, the validity of present pressure ulcer classifica-
tions has to be questioned, because, as stated previously, dif-
ferent etiologies lead to different clinical appearances. Tissue
breakdown due to pressure and/or shear always starts in the
muscle and/or subcutaneous fat, while superficial skin ulcers
are caused by friction in combination with other factors detri-
mental to the skin. In other words, superficial skin lesions pos-
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sibly located over bony prominences and caused by friction
and/or moisture must not be classified as pressure ulcers, be-
cause pressure played no role. Although this issue is the topic
of frequent discussion, consensus has not yet been
achieved.40,41 Also, from a histological point of view, distin-
guishing between superficial pressure ulcers and moisture le-
sions is impossible.42 On the other hand, empirical evidence
exists that superficial skin lesions (grade 2/Stage II pressure
ulcers) can be caused by pressure; however, cited studies18,30,42,43
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focused on the skin only. Arao et al44 described complete de-
cline of epidermis and dermal papillae in a grade 2/Stage II
pressure ulcer, but neither the main cause (pressure, shear, or
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friction) was known nor deeper tissue beneath the superficial
skin lesion examined. Investigations that include all tissue lay-
ers (ie, superficial skin to subcutaneous fat, fascia, and muscle)
are rare. Based on the existing literature, one conclusion ap-
pears obvious: When superficial skin lesions due to compres-
sion are visible, muscle or subcutaneous fat damage must have
taken place because deeper tissue is more vulnerable to pres-
sure forces.11,14,17,19,26-28
Although the distinction between superficial pressure ul-
cers and moisture-related lesions seems to be difficult for both
DO
etiological and clinical reasons, some authors argue that a cor-
rect differentiation is important because pressure ulcers
should be recorded as clinical incidents and are interpreted as
an adverse event in patient care, which has regulatory conse-
quences.41,45 This triggers further questions: First, does this
mean that other skin problems such as incontinence-related
24 OSTOMY WOUND MANAGEMENT SEPTEMBER 2009
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dermatitis or damages due to tape removal are not incidents?
Assuming this is true, how should suspected large proportions
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of false-positive and false-negative judgments of superficial
pressure ulcers (as discussed in the systematic review and four
empirical studies, mentioned previously) be handled? Regard-
less of the liability implications of both questions, conceptual
definitions and diagnostic instruments that take the actual
complexity of superficial skin lesion development into ac-
count but do not cause additional uncertainty are needed.
Extensive destruction and necrosis of deeper tissue due to
OD
long-enduring unrelieved pressure is a well-known phenom-
enon. A clinically relevant concern is that hours or days after
that injury, skin alterations may or may not be visi-
ble.16,19,26,27,40,46,47 Therefore, classifying these lesions correctly
hardly seems possible until the full extent of tissue damage
can be seen. After all, is it really possible to distinguish between
grade1/Stage I pressure ulcers and deep tissue injuries when
the skin is intact? Although the clinical relevance and course
of grade 1/Stage I pressure ulcers are yet not fully understood,
it can be assumed that deeper tissue layers already are involved
when grade1/Stage I pressure ulcers are visible.14,32,48-50 Fur-
thermore, not all deep tissue injuries progress to full-thickness
defects.6,51
How Can Conceptual Problems Be Solved?
Pressure ulcer development is a complex phenomenon; it is
apparent that superficial and deep ulcers have different etiolo-
gies. Unequivocal definitions as well as classifications of pressure
ulcers should clearly characterize these kinds of lesions.
One possible solution would be to exclude grade 2/Stage II
pressure ulcers from the current classifications to overcome
the conceptual problems regarding superficial skin lesions. In-
stead, they should be labelled as friction or moisture lesions.
In that case, only grade 3/Stage III and Stage IV ulcers would
be real pressure ulcers caused by pressure. However, this pro-
vides only a theoretical solution because in clinical practice,
pressure, shear, and friction forces usually coexist. For exam-
ple, when patients are highly care dependent — ie, persons
with restricted mobility and activity and moist skin — de-
velop tissue lesions, it is difficult to determine the main etiol-
ogy with certainty. According to the available EPUAP and
NPUAP definitions, without knowing the exact etiology, it is
impossible to decide whether the lesion is a pressure ulcer.
Consequently, when clinicians are not sure whether such tis-
sue damage is caused by pressure, the lesion should not be
termed pressure ulcer. A more general term such as decubitus
ulcer, as provided by the ICD-10, would be more appropriate.
The authors’s experience has shown that in clinical practice
it often is difficult to establish the distinct causes when decu-
bitus ulcer-like wounds occur. Therefore, it would be logical
to exclude etiology from future definitions. Focusing on clinical
signs and symptoms may be more promising in enhancing di-
agnostic accuracy, as long as the treatment remains independ-
ent of the etiology. The authors suggest classifying decubitus
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Table 1. Description of pressure ulcer classifications

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Shea34 EPUAP9 NPUAP10

Grade 1: Most apparent Grade 1: Nonblanchable Stage I: Intact skin with nonblanchable redness of a localized area
clinical presentation is an erythema of intact skin. usually over a bony prominence. Darkly pigmented skin may not
irregular, ill-defined area of Discoloration of the have visible blanching; its color may differ from the surrounding
soft tissue swelling and in- skin, warmth, edema, area. Further description: The area may be painful, firm, soft,
duration with associated induration, or hardness warmer or cooler as compared to adjacent tissue. Stage I may
heat and erythema overly- also may be used as be difficult to detect in individuals with dark skin tones. May indi-
ing a bony prominence. indicators, particularly cate “at risk” persons (a heralding sign of risk)

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Extreme Grade 1 is a on individuals with
moist superficial irregular darker skin
ulceration limited to epi-
dermis, exposing underly-
ing dermis and resembling
an abrasion. Anatomic
limit: dermis

Grade 2: Clinically pre- Grade 2: Partial-thick- Stage II: Partial-thickness loss of dermis presenting as a shallow
sented as a shallow full-
thickness skin ulcer, the
edges of which are more
distinct. Anatomic limit:
subcutaneous fat
epidermis, dermis, orPR
ness skin loss involving open ulcer with a red-pink wound bed, without slough. Also may

both. The ulcer is su-

perficial and presents
clinically as an abra-
present as an intact or open/ruptured serum-filled blister. Further
description: Presents as a shiny or dry shallow ulcer without
slough or bruising.* This stage should not be used to describe
skin tears, tape burns, perineal dermatitis, maceration, or excori-
sion or blister ation. *Bruising indicates suspected deep tissue injury

Grade 3: Irregular full thick- Grade 3: Full-thickness Stage III: Full-thickness tissue loss. Subcutaneous fat may be vis-
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ness skin defect extending skin loss involving ible but bone, tendon, or muscle are not exposed. Slough may
into the subcutaneous fat damage to or necrosis be present but does not obscure the depth of tissue loss. May
exposing a draining, foul- of subcutaneous tissue include undermining and tunneling. Further description: The
smelling, infected, necrotic that may extend down depth of a Stage III pressure ulcer varies by anatomical location.
base that has undermined to, but not through, un- The bridge of the nose, ear, occiput, and malleolus do not have
the skin for a variable dis- derlying fascia subcutaneous tissue and Stage III ulcers can be shallow. In con-
tance. Anatomic limit: trast, areas of significant adiposity can develop extremely deep
deep fascia Stage III pressure ulcers. Bone/tendon is not visible or directly
palpable
Continued on next page
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ulcers into two broad categories: 1) superficial ulcers and 2) While the proposed solution might be too simple for some
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deep ulcers. This distinction would have advantages: it is simple
and simplicity enhances diagnostic accuracy and reliability.35
It avoids any kind of assumptions regarding etiology, especially
the difficult distinction between pressure and moisture lesions.
Avoiding the terms stages or grades clarifies that both categories
(superficial and deep) can develop independently from each
other and that deep ulcers are not necessarily a progression
from superficial ulcers. Additionally, the category unstageable,
proposed by the NPUAP, becomes redundant, because the
ulcer can be classified as deep. Finally, the authors recommend
DO
circumstances, such as research, the importance of pressure
ulcer classifications in clinical practice may be overestimated.
Grading tissue lesions according to the available pressure ulcer
classifications provides only minor guidance for treatment —
general wound management principles including assessment
of the presence of devitalized or necrotic tissue, inflammation
or infection, moisture, characteristics of the wound edge, and
measurement of the wound size are much more important for
guiding care.52,53 Specification of the anatomical depth of the
tissue damage according to currently used pressure ulcer clas-

use of the term nonblanchable erythema (grade 1/Stage I pres-
sure ulcers) and suspected deep tissue injuries as important
clinical warning signs for subsequent tissue breakdown. Oc-
currence of these signs should indicate an urgent need for pre-
ventive measures; however, such skin impairments should not
be classified as ulcers until tissue damage is visible.
sifications seems to be more suitable for outcome measures
or endpoints in clinical trails.
Conclusion
The recommendations made in this article may provide a
means to overcome diagnostic problems and uncertainty in

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Table 1. Description of pressure ulcer classifications continued

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Shea34 EPUAP9 NPUAP10

Grade 4: Clinical presenta-
tion resembles that of a
Grade 3 except that bone
can be identified in the
base of the ulceration,
which is more extensively
undermined with profuse
Grade 4: Extensive de- Stage IV: Full-thickness tissue loss with exposed bone, tendon, or
struction, tissue necro- muscle. Slough or eschar may be present on some parts of the
sis, or damage to wound bed. Often includes undermining and tunneling. Further
muscle, bone, or sup- description: The depth of a Stage IV pressure ulcer varies by
porting structures with anatomical location. The bridge of the nose, ear, occiput, and
or without full-thick- malleolus do not have subcutaneous tissue and these ulcers can
ness skin loss be shallow. Stage IV ulcers can extend into muscle and/or sup-

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drainage and necrosis. porting structures (eg, fascia, tendon, or joint capsule) making
Anatomic limit: no limit osteomyelitis possible. Exposed bone/tendon is visible or directly
palpable

Closed pressure sores: Is- Suspected deep tissue injury: Purple or maroon localized area of
chemic necrosis in the discolored intact skin or blood-filled blister due to damage of un-
subcutaneous fat without derlying soft tissue from pressure and/or shear. The area may be
skin ulceration leading to preceded by tissue that is painful, firm, mushy, boggy, warmer, or
the development of a cooler as compared to adjacent tissue. Further description: Deep
bursa-like cavity filled with
necrotic debris. Resem-
bling a Grade 3 sore in ex-
tent and depth. Overlying
pigmented, thickened, and
PR tissue injury may be difficult to detect in individuals with dark skin
tones. Evolution may include a thin blister over a dark wound
bed. The wound may further evolve and become covered by thin
eschar. Evolution may be rapid, exposing additional layers of tis-
sue even with optimal treatment
fibrotic skin eventually
ruptures, creating a small Unstageable: Full-thickness tissue loss in which the base of the
skin defect draining a ulcer is covered by slough (yellow, tan, gray, green, or brown)
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large base. Anatomic limit: and/or eschar (tan, brown or black) in the wound bed. Further
deep fascia description: Until enough slough and/or eschar is removed to ex-
pose the base of the wound, the true depth, and therefore stage,
cannot be determined. Stable (dry, adherent, intact without ery-
thema or fluctuance) eschar on the heels serves as “the body's
natural (biological) cover” and should not be removed

Am J Nurs. 1949;49:688–690.
clinical practice when caring for patients with lesions and 5. Conway H, Griffith BH. Plastic surgery for closure of decubitus ulcers in
wounds that present within the context of skilled care. How- patients with paraplegia. Am J Surg. 1956;91:946–975.
T

6. Kosiak M. Etiology of decubitus ulcers. Arch Phys Med Rehabil.

ever, some questions require further investigation. The term
1961;42:19–29.
decubitus ulcer needs more conceptual clarity — ie, what is a 7. National Library of Medicine – Medical Subject Headings. MeSH De-
decubitus ulcer? What are the etiologic factors, clinical course, scriptor Data 2009. Available at:
NO

and prognosis for lesions in the different categories? Which
differentiation is most relevant for clinical decision-making?
Answers to these questions are necessary for the develop-
ment and evaluation of evidence-based diagnostic instru-
ments that facilitate choice of effective, individually targeted
prevention and treatment strategies. Validity of taxonomies
used in databases or in the ICD-10 could be improved; obvi-
ously, decubitus ulcers are not the only diseases of the skin.
Answers are forthcoming only through multidisciplinary
communication and research. ■
DO
www.nlm.nih.gov/cgi/mesh/2009/MB_cgi?mode=&term=Pressure+Ulce
r&field=entry. Accessed September 1, 2009.
8. World Health Organisation (WHO). International Statistical Classification
of Diseases and Related Health Problems 10th Revision. 2007. Available
at: www.who.int/classifications/apps/icd/icd10online/. Accessed Sep-
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Accessed September 1, 2009.
10. National Pressure Ulcer Advisory Panel (NPUAP). Pressure Ulcer Stages
Revised by NPUAP. 2007. Available at: www.npuap.org/pr2.htm. Ac-
cessed September 1, 2009.
11. Daniel RK, Priest DL, Wheatley DC. Etiologic factors in pressure sores:

an experimental model. Arch Phys Med Rehabil. 1981;62:492–498.

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