The Diabetic Foot Syndrome Diagnosis and Consequences

The Diabetic Foot Syndrome,

diagnosis and consequences

RIJKSUNIVERSITEIT GRONINGEN

The Diabetic Foot Syndrome,

diagnosis and consequences

Proefschrift

ter verkrijging van het doctoraat in de
Medische Wetenschappen
aan de Rijksuniversiteit Groningen
op gezag van de
Rector Magnificus, dr. F. Zwarts,
in het openbaar te verdedigen op
woensdag 6 november 2002
om 16.00 uur

door

Johannes Wilhelmus Gerardus Meijer

geboren 21 januari 1966
te Hulst

Promotores Prof. drs. W.H. Eisma
Prof. dr. J.W. Groothoff

Co-promotores Dr. T.P. Links
Dr. A.J. Smit

Beoordelingscommissie Prof. dr. J.H. Arendzen
Prof. dr. R.O.B. Gans
Prof. dr. J.A. Lutterman

voor Miriam

paranimfen H.R. Schiphorst Preuper
F. de Laat

Correspondence Rehabilitation Centre Tolbrug
Tolbrugstraat 11
PO Box 90153
5200 ME 's-Hertogenbosch
the Netherlands
tel: +31-73-6992118/2128
fax: +31-73-6992895

Printed by Ponsen & Looijen BV,
Wageningen, the Netherlands

Cover drawings Christiaan en Roeland Meijer

The publication of this thesis is financially supported by:
Novo Nordisk Farma BV, OIM Groep, Diabetes Fonds,
Vereniging Beatrixoord Haren, Coloplast BV, LIVIT Orthopedie,
Basko Health Care BV, Maatschap Revalidatiegeneeskunde Den Bosch

Meijer, Jan-Willem G.
The diabetic foot syndrome, diagnosis and consequences.
Thesis University of Groningen, the Netherlands – With ref. – With summary in
Dutch.

ISBN-number 90-77113-06-1

© 2002: J.W.G. Meijer, Vlijmen, the Netherlands.
All rights reserved. No parts of this publication may be printed or utilized in any
form by any electronic, mechanical or other means, now known or hereafter
invented, including photocopying and recording, or in any information storage or
retrieval system, without written permission of the copyright holder.

Contents
Chapter 1 Introduction and outline of the thesis 1

Chapter 2 Evaluation of a screening and prevention
programme for diabetic foot complications 11

Chapter 3 Quality of life in patients with
diabetic foot ulcers 23

Chapter 4 Symptom scoring systems to diagnose distal
polyneuropathy in diabetes:
the Diabetic Neuropathy Symptom score 35

Chapter 5 Diabetic Neuropathy Examination:
a hierarchical scoring system to diagnose
distal polyneuropathy in diabetes 51

Chapter 6 Clinical diagnosis of diabetic polyneuropathy
with the DNS and DNE score 63

Chapter 7 Early polyneuropathy in diabetes:
concurrent sensory and motor disturbances 77

Chapter 8 Dissociation in polyneuropathy and
cardiovascular autonomic neuropathy
in diabetes mellitus 91

Chapter 9 Discussion and conclusions 107

Summary 127

Samenvatting 133

Northern Centre for Healthcare Research (NCH)
and previous dissertations 139

Dankwoord 145

Curriculum Vitae 151

Chapter 1

Introduction and outline of the thesis

2 - The diabetic foot syndrome

1.1 Introduction

A very disabling long-term complication of diabetes mellitus (DM) is the
diabetic foot syndrome. The diabetic foot syndrome can be defined as an
array of foot abnormalities, resulting from peripheral neuropathy, macro-
angiopathy and other consequences of metabolic disturbances 1. These
different causal factors may be present alone, but mostly occur in
combination in patients with DM. Neuropathy, particularly symmetric distal
polyneuropathy, is the major etiological factor, and is present in 85% of the
patients with a diabetic foot problem 2. A clinical important manifestation of
the diabetic foot syndrome is the diabetic foot ulcer, sometimes followed by
amputation.

In 2000, worldwide 157 million people are suffering from DM, of which
about 20 million in Europe 3. In 1994 the prevalence of DM in the
Netherlands among men and women of 20 years and older was estimated to
be 33.4/1000, and 42.5/1000, respectively, leading to 442.300 people with
DM 4. About 50% of these people are undiagnosed 4. Type 2 DM is most
frequent, with a presence of 80-90%, type 1 DM is present in 10-20% of the
population 4. As a sequence of demographic changes of the Dutch society, as
there are growth of the population and changes in age and sex distribution,
the prevalence of DM will increase with 35-45% during the period 1994-
2015 5. This increase will be even higher due to the development of more
adequate case finding/screening techniques and the tendency of increasing
incidence rates in certain population subgroups 5.
An ulcer will affect 15-25% of all individuals with diabetes at least once in
their lifetime, with an annual incidence of 2 - 3% 6,7. A cross-sectional study
in 4 general practitioner practices in the Netherlands showed that the
prevalence of an infected foot lesion or ulcer in patients with diabetes was
3% 8. An other study showed that 5% had an ulcer or had undergone an
amputation 9. Thus, diabetic foot problems are common in our society.

The relative risk of diabetes related lower extremity amputation has been
reported to vary between 10 (United Kingdom) and 40 (USA) 10,11. The
incidence of amputation in the Northern part of the Netherlands has been
studied by van Houtum et al. and Rommers et al. Van Houtum found an age-
adjusted incidence rate of 8/100.000 in the non-diabetic population and
345/100.000 in the diabetic population in the province of Groningen in 1991-
1992, with a relative risk for patients with DM of 45 12. The percentage of
amputations due to diabetes was 62%. For the entire Dutch population, the
age adjusted incidence in the non-diabetic population was 12/100.000, for the
diabetic population 250/100.000, with a relative risk of 20 12. The percentage
of amputations due to diabetes was 47%. Rommers et al. found an incidence

Chapter 1: Introduction and outline - 3

rate of amputations of 18-20/100.000 in the northern region of the
Netherlands 13. This rate was rather constant from 1982-1994 and showed no
sharp decrease in frequency despite new techniques such as used in
intervention radiology and in vascular surgery. Unfortunately, the
contribution of diabetes is not known in these data.
Apelqvist et al. showed that the recurrence of foot ulcers after 1, 3 and 5
years of observation was 34%, 61% and 70% in diabetic patients with
previous foot ulcers, respectively. The long-term survival after amputation
was 80%, 59%, and 27% after 1, 3 and 5 years of observation. In patients
with primary healed ulcers, without the need of amputation, this was 92%,
73% and 58%, respectively14. Once amputated, 30-50% of the patients
undergo amputation of the contralateral leg within 3 years 15.

This leads to a major burden both on the patient and the health care system.
The risk of amputation is a life long threat to the diabetic patient, and the
costs due to diabetic ulcers and amputation are high. In 1989, 3790 patients
were hospitalised due to diabetic foot ulcer in the Netherlands, costs of
hospital stay only already were estimated 45 million euro16. In 1992, 1810
amputations were performed in diabetic patients, the medical costs were
estimated 20 million euro, costs of absenteeism and rehabilitation were not
taken into account 17. Ragnarson-Tennvall and Apelqvist studied the cost-
effectiveness of the management of diabetic foot ulcers 18. Although
methodological aspects caused difficulties in comparing results between
countries and settings, they state that treatment alternatives in which the limb
is saved are more effective according long-term economic and quality of life
aspects.

Frequent assessment of risk factors is necessary for early detection of patients
at risk, followed by strict diabetes regulation, patient education about foot
care and appropriate footwear 1. These measures can reduce or even prevent
amputations for diabetic foot disease 19. Bakker et al. evaluated the
effectiveness of a Dutch diabetic foot clinic 20. Co-ordinated screening,
prevention and multidisciplinary treatment at this specialised clinic resulted
in a decrease in number and duration of hospital admissions due to foot
ulcers. Furthermore, a reduction was found in amputations of 43% 20.
Edmonds et al. achieved healing in 86% of neuropathic ulcers and 72% of
ischaemic ulcers, and a reduction of 50% of amputations, with a specialised
foot clinic21.

This is also the goal of the St. Vincent declaration 1989: a reduction of 50%
of amputation in diabetic patients.
The high number of amputations in patients with DM in the Northern part of
the Netherlands, more specific in the province of Groningen, illustrated that


there was an urgent need to evaluate the care for the diabetic foot in that
region. In the early nineties, no specific screening and prevention
programmes existed, and foot complications were treated by various
specialists, without multidisciplinary attunement.

At the University Hospital Groningen, the care for diabetic foot disorders
became more organised after starting a study in 1993. In this study, the
Departments of Rehabilitation Medicine, Internal Medicine and
Endocrinology were collaborating. This resulted in this thesis and in a
multidisciplinary approach of the diabetic foot in the University Hospital.

This present study focuses on the extent of the problem of the diabetic foot
syndrome, the consequences of the diabetic foot syndrome on quality of life,
the development of tests to diagnose diabetic neuropathy, and the relation
between neuropathy and angiopathy in diabetes.


1.2 Aims of the study and outline of the thesis

This study was performed at the diabetes outpatient clinic of the Department
of Endocrinology of the University Hospital Groningen, and at the
Department of Diabetes and Vascular Diseases of the Rehabilitation Centre
Beatrixoord, to investigate the following questions:

1 How many patients from the diabetes outpatient clinic of a University
Hospital, unknown with diabetic foot complications, are at risk to develop
these complications and what is their actual state of prevention?

In chapter 2 the current diabetic foot screening and prevention programme of
the diabetes outpatient clinic of the University Hospital Groningen has been
evaluated. Therefore, 50 patients with diabetes mellitus, unknown with foot
complications, were selected at random to assess a risk-profile and the
preventional status. The aim was to get insight in the extent of the local
population at risk and to form a basis for further development and
organisation of diabetic foot care at our hospital and rehabilitation centre.

2 What is the influence of having a present or former foot ulcer on the quality
of life of patients with diabetes mellitus?

In chapter 3 quality of life was measured in a group of diabetic patients with
present or former foot ulcers and compared with diabetic patients unknown
with foot complications. Quality of life was studied on the domains physical,
social and psychological functioning. Special attention was paid to mobility
and physical disabilities because of expected limitations on these items.

3 Is it possible to modify the Neuropathy Symptom Score (NSS) and the
Neurological Disability Score (NDS) into valid, easily managed, graded and
accurate scoring systems for diagnosing distal symmetric polyneuropathy in
diabetes mellitus?

Neuropathy, especially distal symmetric polyneuropathy, is a major
etiological factor in diabetic foot complications; in 85% of the diabetic
patients with ulcers neuropathy is present. Because of the lack of a gold
standard to diagnose neuropathy, the San Antonio Consensus Statement of
1988 recommended to perform at least one measurement of 5 different
diagnostic categories, including a symptom score and a physical examination


score. Several scores are used, the Neuropathy Symptom Score (NSS) and
the Neurological Disability Score (NDS) are the most accepted scores. Both
are scores for neuropathy in general and not specific for distal symmetric
polyneuropathy. The aim of this study was to adapt the NSS and NDS into
valid, easily managed, graded and accurate scoring systems for diagnosing
distal symmetric polyneuropathy. These studies are described in chapter 4, 5
and 6, respectively.

4 Is polyneuropathy present in patients with DM before any sign of micro- or
macroangiopathy is detectable? Does sensory polyneuropathy occur prior to
motor neuropathy or do they occur simultaneously?

In the pathogenesis of diabetic neuropathy a vascular and a metabolic
hypothesis exist. In this study, presence of sensory and motor polyneuropathy
was evaluated in diabetic patients without micro- or macroangiopathy.
In distal symmetric polyneuropathy, sensory dysfunction seems to run ahead
of motor dysfunction, because of compensating mechanisms, such as
collateral innervation and muscle fiber hypertrophy. Invasive muscle fiber
conduction velocity (I-MFCV) offers sensitive information about muscle
fiber volume and conduction velocity, and thus of early denervation. In
chapter 7, I-MFCV was used as an indicator for early motor dysfunction in
diabetic patients.

5 Do cardiovascular autonomic neuropathy tests reflect diabetic
polyneuropathy or diabetic vasculopathy?

The frequently used Ewing Battery is known to have a high predictive value
in the development of diabetic foot complications. The San Antonio
Consensus Statement recommends cardiovascular autonomic neuropathy
(CAN) tests, as one of the five different categories for diagnosing diabetic
neuropathy. However, evidence exists that the association with other
diagnostic categories for neuropathy is weak, and that CAN is more strongly
related to vasculopathy in diabetes mellitus. Recently, new methods have
been developed to measure CAN, such as Heart Rate Variability (HRV) and
Baroreflex Sensitivity (BRS). In chapter 8 these tests for cardiovascular
dysfunction were studied, and compared with conventional tests for distal
symmetric polyneuropathy and vascular examination.


1.3 References

1 Syllabus Richtlijnen diabetische retinopathie, diabetische nefropathie,
diabetische voet en hart en vaatziekten bij diabetes mellitus.
Richtlijnen NDF/CBO september 1998. Banda Heerenveen BV, the
Netherlands.
2 Boulton AJM. The pathogenesis of diabetic foot problems: an
overview. Diabet Med 1996; 13: 12-16.
3 Post D, Tuinstra J, Groothoff JW. Zorgconsumptie van patiënten met
diabetes mellitus. Tijdschrift voor Gezondheidswetenschappen 2000;
78 (6): 354-60.
4 Volksgezondheid Toekomst Verkenning 1997, I De
gezondheidstoestand: een actualisering.
5 Volksgezondheid Toekomst Verkenning 1997, De som der delen.
6 Palumbo PJ, Melton LJ. Peripheral vascular diseases and diabetes. In:
Harris MI, Hamman RF, eds. Diabetes in America. NIH publication
No. 85-1468. Washington: US Government Printing Office, 1985: XV
1-21.
7 Most R, Sinnock P. The epidemiology of lower extremity amputations
in diabetic individuals. Diabetes Care 1983; 6: 87-91.
8 Crebolder HFJM. De huisarts en de diabetische voet. In: Consensus
bijeenkomst diabetische voet. Utrecht: CBO, 1985: 2-11.
9 Verhoeven S, Ballegooije E van, Casparie AT. Impact of late
complications in type II diabetes in a dutch population. Diabet Med
1991; 8: 435-8.
10 Gujral JS, McNally PG, O'Malley BP, Burden AC. Ethnic differences
in the incidence of lower extremity amputation secondary to diabetes
mellitus. Diabet Med 1993; 10: 271-74.
11 Connel FA, Shaw C, Will J. Lower extremity amputations among
persons with diabetes mellitus. Washington, 1988. MMWR 1991; 40:
737-39.
12 Houtum van WH, Lavery LA. Regional variation in the incidence of
diabetes-related amputations in the Netherlands. Diabetes Res and Clin
Practice 1996; 31: 125-32.
13 Rommers GM, Vos LDW, Groothoff JW, Eisma WH. Epidemiology
of lower limb amputees in the north of the Netherlands: Aetiology,
discharge destination and prosthetic use. Prosthetics and Orthotics
International 1997; 21: 92-99.
14 Apelqvist J, Larsson J, Agardh CD. Long-term prognosis for diabetic
patients with foot ulcers. J of Internal Medicine 1993; 233: 485-91.


15 Bild DE, Selby JV, Sinnock P, Browner WS, Braveman P, Showstack
JA. Lower-extremity amputation in people with diabetes.
Epidemiology and prevention. Diabetes Care 1989; 12: 24-31.
16 Bouter KP, Storm AJ, Groot RR de, Uitslager R, Erkelens DW,
Diepersloot RJA. The diabetic foot in Dutch hospitals: epidiological
features and clinical outcome. Eur J Med 1993; 2(4): 215-18.
17 Houtum van WH, Lavery LA, Harkless LB. The cost of diabetes-
related lower extremity amputations in the Netherlands. Diabet Med
1995; 12: 777-781.
18 Ragnarson-Tennvall G, Apelqvist J. Cost-effective management of
diabetic foot ulcers, a review. Pharmaco-economics 1997; 12 (1): 42-
53.
19 Assal JP, Muhlhauser I, Pernat A, Gfeller R, Jorgens V, Berger M.
Patient education as the basis for diabetic care in clinical practice.
Diabetologia 1985; 28: 602-13.
20 Bakker K, Dooren J. Een gespecialiseerde voetenpolikliniek voor
diabetespatienten vermindert het aantal amputaties en is
kostenbesparend. NTvG 1994; 138(11): 565-69.
21 Edmonds ME, Blundell MP, Morris ME, Thomas EM, Cotton LT.
Improved survival of the diabetic foot: the role of a specialized clinic.
Q J Med 1986; 60 (232): 763-71.


Chapter 2

Evaluation of a
screening and prevention programme for
diabetic foot complications

J.W.G. Meijer, T.P. Links, A.J. Smit,
J.W. Groothoff, W.H. Eisma

Prosthetics and Orthotics International 2001; 25: 132-38.

© 2001 by ISPO; reprinted with their kind permission

Abstract

Introduction Foot complications in diabetes can be decreased by
preventive measures. The current diabetic foot screening
and prevention programme of the diabetes outpatient
clinic of a university hospital was evaluated, by assessing
the presence of risk factors for the development of foot
disorders and the preventive measures taken.
Methods 50 diabetic patients not known to have foot complications
were selected at random. Risk factors and preventive
measures were inventarised with the Coleman risk-
categorisation system and the Preventive Measures Scale,
respectively.
Results 60% of the patients were at risk of developing diabetic
foot complications. The preventive measures were low in
these patients. Patient knowledge was insufficient and
behaviour even worse. Basal preventive shoe adaptations
were absent in most patients at risk. No relation between
risk category and the preventional status was found.
Discussion Cross-sectional examination at a university outpatient
clinic showed serious risk profiles for foot complications,
which were not balanced by the application of generally
accepted preventive measures. At the outpatient clinic,
screening should be optimised.


2.1 Introduction

Foot complications have an enormous impact on the quality of life of patients
with diabetes mellitus and the financial cost is considerable 1,2. Frequent
assessment of risk factors (neuropathy, foot deformity, history of ulceration
and angiopathy) is necessary for the early detection of patients at risk for
developing foot disease and for preventing amputation. Better patient
education about foot care and appropriate footwear are expected to prevent at
least half of the amputations for diabetic foot disease 3-7.
At the time of this study, standardised diabetes patient education with the
usual attention to diabetic foot care was being given at the university
outpatient clinic. This individual education is repeated every two years and
the feet are examined once a year or more frequently on indication.
The aim of this study was to evaluate the clinic's current screening and
prevention programme by assessing the risk profile and the actual state of
prevention in a sample of patients, not known to have diabetic foot
complications, at the outpatient clinic. The information was intended to form
a basis for further development and organisation of diabetic foot care at the
hospital and rehabilitation centre.

2.2 Patients and Methods

Patients
At the diabetes outpatient clinic of the University Hospital Groningen, 55
patients who had been suffering from diabetes mellitus for at least one year,
but did not have any documented foot complications, were selected at
random. Exclusion criteria were: causes of neuropathy other than diabetes
mellitus, other neurological diseases or peripheral nerve disorders, high dose
benzodiazepine or analgesic use, cognitive or psychological problems as far
as they might interfere with the test results, the presence or a history of foot
ulceration and foot amputation.
Five patients refused to take part in this research project.

Methods
The same specialist (JWGM) examined all 50 patients. In the same session,
risk factors and preventive measures were assessed using a risk-
categorisation system and the Preventive Measure Scale, respectively.
Patients were not informed about the results of the tests.

Chapter 2: Evaluation of screening and prevention - 13

1 Coleman's risk categorisation
No generally accepted risk profile is available to determine a patient's risk of
developing foot problems. The American Diabetes Association (ADA)
recommends assessment of the four major risk factors: neuropathy, foot
deformity, ulceration and angiopathy 8.

As risk profile, Coleman's risk-categorisation system was chosen 9, which
covers these major risk factors. Four different risk categories are used (see
Table 1). In risk category 0 the only risk factor present is foot deformity. In
category 1 neuropathy is present. In category 2 the presence of neuropathy is
combined with foot deformity, while in category 3 angiopathy or an ulcer are
present.

Table 1: Risk profile according to Coleman 9
risk category 0 1 2 3
Neuropathy - + + +
Foot deformity -/+ - + +
Ulceration and/or vascular laboratory - - - +
findings implying angiopathy
Number of patients (%) 20 10 4 16
(40%) (20%) (8%) (32%)

1a Neuropathy
According to the recommendations of the ADA, the presence of neuropathy
was determined with Semmes Weinstein Monofilaments (SWMF) and the
Vibration Perception Threshold (VPT) 10. These are semi-quantitative,
reliable instruments, complementary to each other, with proven predictive
value for the development of clinical problems, such as foot ulcers and the
need for amputation 11-18. Both were applied 6 times to two locations on both
feet. Insensitivity to the 10 gram SWMF was scored as absence of protective
sensibility. The VPT was determined with a hand-held biothesiometer
(Biomedical Instruments Inc., Ohio, USA) and compared to the reference
values published by Young et al.17. Neuropathy was defined as a disturbed
VPT and/or insensitivity to the 10-gram SWMF at one location or more.

1b Foot deformity
Foot deformity was defined as comprising at least one of the following
obvious deformities: claw toes, overlying toes, prominent bony parts and
hallux rigidus or valgus.


1c Ulceration
Patients with ulceration or a history of ulceration were excluded from this
study.

1d Angiopathy
In Coleman's system, angiopathy is defined as vascular laboratory findings
indicating significant angiopathy. Ankle/brachial indexes at the arteria
dorsalis pedis and arteria tibialis posterior and toe/brachial indexes at the
hallux on both sides using laser-doppler flowmetry, were measured.
Ankle/brachial indexes of below 0.90 and toe/brachial indexes of below 0.75
were considered abnormal 19. Angiopathy was diagnosed if one or more
abnormal value was observed.

2 The Preventive Measures Scale
According to recommendations of the American Diabetes Association,
diabetic patients should be educated regarding their risk factors and
appropriate management 10. Assessment of a person's current knowledge and
care practices should be obtained. Patients should understand the implications
of the loss of protective sensation, the importance of foot monitoring on a
daily basis, the proper care of the foot, including nail and skin care, and the
selection of appropriate footwear. It is known that the type of evidence for the
effectiveness of these specific interventions varies, ranging from evidence
based (randomised controlled trials) for prescription of adequate footwear to
expert or consensus opinions of the other interventions.
In literature there is no valid score available to quantify the preventive status
of these patients. Therefore, a panel of medical specialists of the University
Hospital, all members of the Diabetic Foot working group, developed the
PMS on expert and consensus opinion regarding the recommendations of the
ADA, several education programmes, guidelines for shoes, and the
literature9,10,20-22.

The PMS has four sub-scales: (1) patient knowledge (7 items), (2) care
practice (9 items), (3) condition of feet and shoes (10 items) and (4)
prevention by health care workers (5 items). Sub-scales 1, 2 and 4 are based
on self-reporting, 3 is based on observation. The PMS is standardised, self-
reporting questions could be answered yes or no. Observation criteria for sub-
scale 3 were described in detail before starting the study. Adequate measures
received 0 points, inadequate measures received 1 point, thus the maximum
score was 31 points. The PMS is shown in Appendix 1.


Statistics
The statistical package SPSS-PC was used for all the analyses, including
computation of the descriptive statistics, Spearman's Correlation Coefficient
and Oneway Multiple Range Test.

2.3 Results

Characteristics of the 50 participants are shown in Table 2. The mean age
was 51.4 years (min 18, max 89 yrs), while the mean duration of DM was
14.1 years (min 1, max 36 yrs). The group consisted of 32 men and 18
women; 22 had type 1 DM and 28 had type 2 DM.

Table 2: Patient characteristics
N 50
mean age (years) (SD) 51.4 (16.2)
min – max (years) 18 – 89
mean duration diabetes (years) (SD) 14.1 (9.1)
min – max (years) 1 – 36
sex
male : female 32:18
type of diabetes
type 1 : type 2 22 : 28
mean HbA1c (%) (SD) 8.6 (1.4)
min – max 6.6 - 13.5

1 Coleman's risk categorisation
60% of the patients had scores that placed them in risk categories 1-3. These
patients were at risk. 40% scored in category 0, which means the lowest risk,
because there were no risk factors (or only the presence of foot deformity
without any other risk factors) (Table 1).

2 Preventive measures
Table 3 presents the mean scores on the sub-scales of the Preventive
Measures Scale for each risk category. A large percentage of the patients
were not taking any preventive measures in any of the four sub-scales. Foot-


care behaviour and foot-care knowledge were inadequate. The scores for
foot-care behaviour were even worse than those for foot-care knowledge.

Basal preventive demands of shoes, such as fitting, presence of seamless
insides and pressure distributing inlays, were absent in most patients at risk,
in 53% (16/30), 67% (20/30) and 70% (21/30), respectively.
No relation was found between the risk category and the preventive measures
scale (Spearman's correlation coefficient 0.24). There were no significant
differences in the scores on the preventive measures scale between the four
risk categories.

Table 3: Preventive Measures Scale
The mean percentage of patients in each category who were not performing
the preventive measure

risk category 0 1 2 3
number of patients 20 10 4 16
1 Patient Knowledge: 39.2 40.0 37.5 46.0
2 Patient Care Practice: 56.7 47.8 56.1 52.0
3 Condition of Feet and Shoes: 56.8 55.2 40.1 63.3
4 Preventive Measures by Health Workers: 68.0 50.0 50.0 61.2

2.4 Discussion

Using Coleman's risk-categorisation system, 60 per cent of the study group
were found to be at serious risk of developing diabetic foot complications,
despite the availability of a screening and education programme. The sample
was recruited at a university hospital outpatient clinic and did not have any
documented foot disorders. Foot-care knowledge and foot-care behaviour
were inadequate. The scores for preventive foot-care behaviour were worse
than those for foot-care knowledge; there was no relation between the sub-
scale prevention and risk category. Protective measures by shoe adaptations
were insufficient. This means that the screening and prevention programme,
even though it follows generally prescribed procedures, is inadequate and that
patients do not comply sufficiently with preventive self-care. This might be


exacerbated by the fact that doctors and patients are inclined to underestimate
foot care. In both doctors and patients thresholds need to be overcome in
examining the feet. In doctors, time is scarce and foot inspection takes time.
Many patients have visual problems, which complicate inspection, and some
have cosmetic objections towards wearing orthopaedic footwear.

The study group was not fully representative of the entire population at the
outpatient clinic, because of the exclusion criteria used. The study group was
younger, did not have any documented foot problems, had a shorter duration
of diabetes mellitus and there were relatively more male patients. The
objection might be raised that the study sample was small and, because it was
university-hospital-based, it was not representative. However, the percentage
at risk was so high that valid conclusions can be drawn about the need for
preventive care, even in this small sample. Similar risk estimates for the
general population will underestimate the situation, because patients with (a
history of) foot ulcers were excluded and because everyone had received
standardised diabetes patient education.

Several validated tests to diagnose and evaluate neuropathy are available in
different diagnostic categories, such as symptom scoring, physical
examination, quantitative sensory testing, electrodiagnostic studies and
autonomic function testing. According to a consensus statement one test from
each of these five diagnostic categories has to be used to diagnose and
evaluate neuropathy 23. In clinical practice, certainly at an outpatient clinic,
this is not feasible for screening purposes. The ADA recently recommended
the use of psychophysical somatosensory threshold tests (especially VPT by
Biothesiometry and SWMF testing) because these tests provide the best
discrimination in the clinical setting to identify the loss of sensation 10. Both
recommended tests have been used in this study. However, there is still no
combination of tests available with the optimal predictive value to diabetic
foot ulcer. By using only these two methods still cases will be missed during
screening, so the percentage at risk will even be higher than 60%.

It is questionable whether the highest risk category should be defined by the
presence of angiopathy. Several studies have shown that neuropathy played a
larger role in the development of ulceration and the need for amputation than
angiopathy 7,20,24-26. This means that for the entire 60% (categories 1-3:
neuropathy present) the risk is high and preventive foot care is of great
importance.

Because there was no score available in literature, the Preventive Measures
Scale was developed to standardise the quantification of the preventive
measures being taken by patients. Validation of the PMS was beyond the


scope of this study. The PMS is not broad enough to evaluate education
programmes, because information about the social system, coping, behaviour
and health locus of control are lacking. However, the PMS does provide a
simple, standardised instrument to assess the preventive measures being
taken by patients. Three sub-scales are based on self-report. Patients might
respond socially desirable, which means that the real situation of prevention
is even worse than reported.

In view of the findings of this evaluation, the screening and prevention
programme has to be revised. Because our programme closely follows
generally accepted programmes, this need for revision will hold for many
institutions. In our opinion, the screening programme needs to be adapted to
follow the advice of the 1998 Dutch consensus on diabetic foot disease 27,
which means more intense examination of the presence of risk factors.
Naturally, to be of any benefit, early diagnosis of patients at risk will have to
be followed by preventive measures and regular check-ups. For this purpose,
a multidisciplinary diabetic foot team and intensive education programmes
have been started at the University Hospital and rehabilitation centre. The
education programme offers information and individual or group training
given by a multidisciplinary rehabilitation team. The major goal of this
programme is to increase the level of preventive self-care.

Physicians, podiatrists and shoe-technicians need to be aware that they will
have to provide adequate footwear to an enormous number of patients at risk.
Furthermore they should underpin their work, specifically the indications and
effects of adaptations and their preventive value.

Using a simple risk-categorisation system combined with improved
prevention strategies for patients at risk of developing diabetic foot problems,
we are attempting to balance the presence of risk factors and the application
of preventive measures. It is clear that patients, health care workers and
health insurance companies will have to invest a great deal of time and
money in foot care to reach the goal of the St. Vincent Declaration, i.e. a 50%
reduction in major amputations.


2.5 References

1 Bakker K, Dooren J. Een gespecialiseerde voetenpolikliniek voor
diabetespatiënten vermindert het aantal amputaties en is
kostenbesparend. NTvG 1994; 11: 565-69.
2 Ollendorf DA, Kotsanos JG, Wishner WJ. Potential economic benefits
of lower-extremity amputation prevention strategies in diabetes.
Diabetes Care 1998; 21:1240-45.
3 Assal JP, Muhlhouser I, Pernet A, Gfeller R, Jorgens V, Berger M.
Patient education as the basis for diabetic foot care in clinical practice.
Diabetologia 1985; 28: 602-613.
4 Edmonds ME, Blundell MP, Morris ME, Maelor TE, Thomas E,
Cotton LT, Watkins PJ. Improved survival of the diabetic foot: the role
of the specialised foot clinic. Quart J of Med 1986; 232: 763-71.
5 Schaff PS, Cavanagh PR. Shoes for the insensitive foot: the effect of a
"rocker bottom" shoe modification of plantar pressure distribution.
Foot Ankle 1990; 11: 129-40.
6 Barth R, Campbell LV, Allen S, Jupp JJ, Chisholm DJ. Intensive
education improves knowledge, compliance and foot problems in type
2 diabetes. Diabet Med 1991; 8: 111-17.
7 Thomson FJ, Veves A, Ashe H, Knowles EA, Gem J, Walker MG. A
team approach to diabetic foot care: the Manchester experience. The
Foot 1991; 2: 75-82.
8 American Diabetes Association. Preventive foot care in people with
diabetes. Diabetes Care 2000; 23: s55-56.
9 Coleman WC. Footwear in a management program for injury
prevention. In: Levin ME, O'Neal LW, Bowker JH (eds). The Diabetic
Foot, 5th edition. St. Louis: Mosby-Year Book, 1993, P 533-36.
10 Mayfield JA, Reiber GE, Sanders LJ, Janisse D, Pogach LM.
Preventive foot care in people with diabetes. Diabetes Care 1998; 21:
2161-77.
11 Goldberg JM, Lindblom U. Standardised method of determining
vibratory perception thresholds for diagnosis and screening in
neurological investigation. J of Neur, Neurosurg and Psych 1979; 42:
793-803.
12 Bloom S, Till S, Sonksen P, Smith S. Use of a biothesiometer to
measure individual vibration thresholds and their variation in 519 non-
diabetic subjects. BMJ 1984; 288: 1793-95.
13 Birke JA, Sims DS. Plantar sensory threshold in the ulcerative foot.
Lepr Rev 1986; 57: 261-67.
14 Sosenko JM, Kato M, Soto R, BiId DE. Comparison of quantitative
sensory-threshold measures for their association with foot ulceration in
diabetic patients. Diabetes Care 1990; 13: 1057-61.


15 Kumar S, Fernando DJS, Veves A, Knowles EA, Young MJ, Boulton
AJM. Semmes Weinstein Monofilaments: a simple, effective and inex-
pensive screening device for identifying diabetic patients at risk of foot
ulceration. Diab Res and Clin Pract 1991; 13: 63-68.
16 Veves A, Uccioli L, Manes C, van Acker K, Komninou H, Philippides
P, Katsilambros N, de Leeuw I, Menzinger G, Boulton AJM.
Comparison of risk factors for foot problems in diabetic patients
attending hospital outpatient clinics in four different European States.
Diabet Med 1994; 11: 709-11.
17 Young MJ, Breddy L, Veves A, Boulton AJM. The prediction of
diabetic neuropathic foot ulceration using vibratory perception
thresholds. Diabetes Care 1994; 17: 557-60.
18 Valk GD, De Sonnaville JJJ, van Houtum WH. The assessment of
diabetic polyneuropathy in daily clinical practice. Muscle and Nerve
1997; 20: 116-18.
19 Conier SA. Role of pressure measurements. In: Bernstein EF (ed).
Vascular Diagnosis, 4th edition. St. Louis: Mosby, 1993, p 486-512.
20 Boulton AJM. Peripheral neuropathy and the diabetic foot. The Foot
1992; 2: 67-72.
21 Edmonds ME, Foster AVM. Diabetic Foot Clinic. In: Levin ME,
O'Neal LW, Bowker JH (eds). The Diabetic Foot, 5th edition. St.
Louis: Mosby-Year Book, 1993, p 599-603.
22 Caputo GM, Cavanagh PR, Ulbrecht JS, Gibbons GW, Karchmer AW.
Assessment and management of foot disease in patients with diabetes.
N Engl J Med 1994; 331: 854-860.
23 American Diabetes Association, American Academy of Neurology.
Report and recommendations of the San Antonio Conference on
Diabetic neuropathy (Consensus Statement). Diabetes Care 1988; 11:
592-97.
24 Boulton AJM, Kubrusly DB, Bowker JH, Gadia MT, Quintero L,
Becker DM, Skyler JS, Sosenko JM. Impaired vibratory perception
and diabetic foot ulceration. Diabet Med 1986; 3: 335-37.
25 Pecaro RE, Reiber GE, Burgess EM. Causal pathways to amputation:
basis for prevention. Diabetes Care 1990; 13: 513-21.
overview. Diabet Med 1996; 13: 12-16.
27 CBO/NDF. Diabetische retinopathie, diabetische nefropathie,
diabetische voet, hart en vaatziekten bij diabetes mellitus. Heerenveen,
the Netherlands: Banda, 1998.


Appendix 1: Preventive Measures Scale
1: Patient Foot-care Knowledge: 7 items
Do you know about the necessity of:
taking special foot care due to diabetes?
daily inspection of the feet to control for presence of ulcers?
daily washing of the feet?
not walking barefoot?
adequate fitting of the shoes?
visit the doctor for wound care?
special shoe demands?

2: Patient Foot-care Practice: 9 items
Do you pay special attention to:
care of the feet?
daily washing of the feet?
the use of oil for the skin?
examine the feet for wounds daily?
the use of a mirror for inspection?
foot inspection by others?
not to walk barefoot?
inspection of the shoes?
wearing seamless stockings?

3: Condition of feet and shoes: 10 items
Observation criteria: scored as:
condition of nails inadequate: fungal infections, inadequate trimming,
ingrown nails
condition of skin inadequate: dry crackled skin, maceration, callus, tinea
pedis
stockings adequate: seamless
fitting of stockings inadequate: pinch off effects
inside of shoes adequate: seamless
fitting of shoes adequate: widest part at MTP-I, length longest toe to shoe
1.5-2 cm, sufficient room at toes
shoe counter adequate: fixation of heel and foot, no slipping
sole adequate: rigid protecting against penetration trauma
distributing inlay adequate: distribution of pressure over entire plantar
surface
rocker bottom adequate: right place, decreasing pressure plantar forefoot

4: Preventive Measures by Health Care Workers: 5 items
Do your health care workers offer:
foot care (by general practitioner)?
foot care (by endocrinologist)?
prescription for special shoes?
urgent visit for wounds?
annual foot inspection?


Chapter 3

Quality of life
in patients with diabetic foot ulcers

J.W.G. Meijer, J. Trip, S.M.H.J. Jaegers, T.P. Links,
A.J. Smit, J.W. Groothoff, W.H. Eisma

Disability and Rehabilitation 2001; 23 (8): 336-340.

© 2001 by Taylor and Francis; reprinted with their kind permission

Abstract

Aim To compare Quality of Life (QoL) between diabetic
patients with (former or present) and without foot ulcers.
Methods Two patient groups of comparable age, sex distribution,
type distribution and duration of diabetes were studied.
Fourteen patients with former or present, but clinically
stable diabetic foot ulcers (DFUs) were examined. The
control group were 24 patients not known to have DFUs.
None of the participants had other diabetic complications
or conditions that would potentially affect QoL. A
diabetic foot risk score and QoL were assessed. QoL was
scored with the RAND-36, the Barthel Score (ADL) and
the Walking and Walking Stairs Questionnaire (WSQ).
Results Marked and significant differences were found in physical
functioning (p<.001), social functioning (p<.05), physical
role (p<.001) and health experience (p<.05) between the
two groups with the RAND-36 and the four sub-scales of
the WSQ (all p<.001). On all these scales, QoL was
significantly poorer in the study group. A correlation was
found between the risk score and QoL (physical
functioning and physical role Spearman's r: -.66, -.56 and
WSQ -.63, -.64, -.67 and -.71, respectively).
Discussion Presence or history of DFUs has a large impact on
physical role, physical functioning and mobility. Physical
impairments especially influenced QoL. Probably, QoL
can be increased by providing attention that will enhance
mobility and by giving advice about adaptations and
special equipment.


3.1 Introduction

A disabling long-term complication of diabetes mellitus (DM) is the diabetic
foot ulcer (DFU), caused by the presence of neuropathy, angiopathy and/or
foot deformity 1. DFUs are common and it is estimated that they affect 15%
of all individuals with DM during their lifetime 2.

Recently, three studies have been published on Quality of Life (QoL) in
patients with DFUs. Rijken et al. 3 studied the association of foot pain with
several other parameters in the field of impairments, disabilities and quality
of life in 29 patients, without controls. There were no patients with ulcers
included. Several clinical variables and four unvalidated functional variables
were assessed on fatigue, functional ability, walking distance and quality of
life. In this study foot pain was related to fatigue, disability in walking and a
lower level of quality of life.
Carrington et al. 4 examined 13 diabetic patients with ulcers, 13 diabetic
patients with a unilateral amputation and 26 controls. They assessed
psychological adjustment to illness (PAIS), anxiety and depression (HAD)
and life satisfaction (QoL ladder) and concluded that the psychological status
of mobile amputees is better than that of the diabetic foot ulcer patients, but
not as good as diabetic controls. They did not assess mobility.
Brod 5 studied quality of life in diabetic patients with foot ulcers and their
caregivers, by semi-structured discussions on the domains of social,
psychological, physical and economic impact. Two groups participated,
consisting of 14 patients and 11 caregivers without a control group. A
negative impact on all domains of QoL was experienced because of the
limitations in mobility caused by the ulcer. The conclusions were group
findings and not based on individual assessments.
In conclusion, QoL in diabetic patients with foot ulcers is greatly influenced
by physical (especially mobility), social and psychological impairments and
disabilities. However, it is not clear which specific domains of QoL are most
affected by DFUs.

The aim of this study was to evaluate the QoL of individual patients with
present or former DFUs by comparing them to DM patients not known to
have DFUs. QoL was defined as "the physical, social and psychological
functioning of the patients as being influenced by disease or therapy", and
was investigated using the sub-items mobility, activities of daily living and
general QoL 6-8.

Chapter 3: Quality of life - 25


Patients
A cross-sectional patient-control study was performed on patients who were
admitted to the Diabetes Department of the Rehabilitation Centre Beatrixoord
between 1993 and 1997. Two groups were composed, a study group with
patients with DM who had been hospitalised because of DFUs and a control
group with patients without any foot problems, who had a diabetes duration
of at least 1 year and had been admitted because of diabetic dysregulation.
Patients were included if they were ambulatory at the time of the study.
Exclusion criteria were: not diabetes related diseases ( neurological or
orthopaedic problems, cardiac or pulmonary problems), diabetes related
problems (severe retinopathy, nephropathy, amputation above the level of the
toes, unstable ulcers on the feet and symptomatic diabetic polyneuropathy)
and cognitive or psychological problems.
During the period studied, 410 patients had been admitted to the department
for various reasons (dysregulation, amputation, instruction and prevention,
ulcers etc). To select patients and controls, the records were read by JT and
checked by JWGM. Referring to the in- and exclusion criteria mentioned, 31
patients were initially selected for the study group and 53 for the control
group. To get informed about the actual state of the patients, their general
practitioners were contacted to check in- and exclusion criteria just before
starting the study. This led to the exclusion of 12 patients of the study group
and 20 of the control group, the reasons are described in Table 1.
Unfortunately 5 patients of the study group and 9 of the controls refused to
take part in the study, resulting in 14 participants of the study group and 24 of
the control group, as shown in Table 1.

Table 1: Patient selection

Study group Control group
initially selected 31 53
5 died 3 died
check general
-12 5 comorbidity -20 15 comorbidity
practitioner
2 moved house 2 moved house
selected 19 33
-5 refused -9 refused
participated 14 24


Methods

Risk profiles for diabetic foot complications were determined and QoL was
assessed. The same observer examined all the patients (JT).

1 Risk Profile
The risk profile test from the Dutch consensus report on the diabetic foot was
used to assess the risk of developing foot complications 1. This profile
employs the known risk factors neuropathy, angiopathy, foot deformity and
ulceration. Risk is graded from 0 (no risk) to 3 (highest risk). In grade 0, none
of the 4 risk factors are present. In grade 1 the only risk factor present is
neuropathy; in grade 2 neuropathy is present combined with angiopathy or
foot deformity, while in grade 3 there is an existing or previous ulcer 1.
Neuropathy was diagnosed with Semmes Weinstein Monofilaments. Inability
to feel the 10-gram filament at 4 plantar locations on the foot was defined as
the presence of neuropathy 9-11. Angiopathy was defined as symptomatic
arterial disease (Fontaine class 2 or higher) and/or absence of arterial foot
pulsations. Foot deformity was defined as the presence of hallux
valgus/rigidus, prominent bony parts or pressure areas. Ulceration was
present when there were Wagner stage 1 to 5 abnormalities 12.

2 Quality of Life
QoL was assessed with the RAND-36, the Barthel Index and the Walking
and Walking Stairs Questionnaire (WSQ).

2.1 RAND-36
The RAND-36 is a general questionnaire for measuring the influence of
health on QoL (physical, psychological and social aspects) 13. It has proven to
be valid and reliable 13. There are 8 domains: physical and social functioning,
emotional and physical impairment of role, mental health, vitality, pain and
experienced health. For each domain there is a minimum score of 0 and a
maximum score of 100. The higher the score, the better the quality of life.

2.2 Barthel Index
The Barthel index is a questionnaire on skills/disabilities of activities of daily
living (ADL), which consists of 10 questions ranging from bowel and bladder
control items to mobility and personal care items 14,15. The maximum score is
20 points (normal); less than 10 points means severely impaired ADL.

2.3 Walking and Walking Stairs Questionnaire
A reliable and valid preliminary version of the Walking and Walking Stairs
Questionnaire (WSQ) was used to evaluate mobility 16,17. This questionnaire
consists of 62 items, divided into 4 hierarchical scales: using stairs (16 items),


walking indoors (18 items), walking outdoors (20 items) and walking
velocity (8 items). Each scale has a maximum of 100 points; the higher the
score, the better the mobility.

Statistics
The statistical package SPSS-PC was used to compute descriptive statistics,
Spearman's correlation coefficient and the Mann Whitney test.
Significance level: p < .05.
Differences on item level were computed by calculating the Effect Size (EF)
( t-tests for means), defined as 18:

MeanA − MeanB SS A + SSB
, where Sp =
Sp (N A − 1) + (N B − 1)

MeanA = mean of group A, MeanB = mean of group B, Sp = Pooled standard deviation,
SSA = sum of squares of group A, SSB = sum of squares of group B, NA = total of group A,
NB = total of group B
Interpretation of the ES: no or trivial effect < 0.20; small effect = 0.20 – 0.49; medium
effect = 0.50 – 0.79; large effect = > 0.79 19.

3.3 Results

Patient characteristics are shown in Table 2. The two groups were found to be
comparable regarding age, sex distribution, known duration and type of DM
(no significant differences).
The patients selected initially for the study (n=31) and control (n=53) groups
were compared to the patients who actually participated in the two groups on
the items sex distribution, age, known duration and type of diabetes. In the
participating control group, the mean duration of diabetes was significantly
longer than that in the excluded group. In the study group with foot ulcers
there were significantly more men than in the group of excluded patients. No
other significant differences were found between the subjects selected
initially and those who actually participated.


Table 2: Patient characteristics

study group control group
n 14 24
Sex (male : female) 10 : 4 13 : 11
Age (years) (mean (SD)) 62.8 (13.8) 58.7 (13.8)
Duration DM (years) (mean (SD)) 11.3 (10.8) 12.8 (12.0)
Type of DM (1 : 2) 3 : 11 10 : 14

1 Risk Profile

A significant difference was found in the risk profile between the two groups
(p-value < .0001). The study group had a higher risk of developing foot
complications (mean score of 3.00; SD 0.0) than the control group (mean
score 0.58; SD 1.10).

2 Quality of Life

2.1 RAND-36

Patients in the study group scored both relevantly and significantly lower
(experienced a lower QoL) than the controls on the domains physical
functioning, social functioning, physical role and health experience, as shown
in Table 3.

On an item level, the most relevant and significant differences (Effect Size)
were present for producing moderate (1.4) and heavy physical effort (1.8),
walking distances of more than 500 metres (1.2) and using stairs (1.4). The
patients also experienced problems with working, especially a lower
productivity (1.1). There were no differences in complaints about pain.


Table 3: RAND-36

study group control group
mean ± SD mean ± SD
Physical functioning 52.1 ± 31.7 ** 90.0 ± 15.9
Social functioning 80.4 ± 27.6 * 96.4 ± 7.8
Physical role 42.9 ± 34.6 ** 83.3 ± 29.2
Emotional role 92.3 ± 14.6 ns 84.7 ± 31.1
Mental health 75.7 ± 19.5 ns 77.2 ± 15.6
Vitality 71.2 ± 16.0 ns 72.3 ± 15.9
Pain 68.7 ± 28.4 ns 76.2 ± 14.3
Health experience 51.1 ± 23.1 * 66.4 ± 14.9

* ** ns
p < .05, p < .001, not significant

2.2 Barthel Index

The study group scored 19.2 points (SD 1.5), and the control group scored
19.8 points (SD 0.5) (not significant).

2.3 WSQ

In all four categories, the study group had significantly lower scores than the
control group, which means that the patients with foot ulceration experienced
more disabilities on mobility than the controls. The study group scored 80.0
points for using stairs versus 96.7 points in the controls (p<.001); for walking
indoors the scores were 54.8 and 90.3 (p<.001), respectively. For walking
outdoors, the study group scored 54.5 points versus 87.0 in the controls
(p<.001), while for walking velocity, these scores were 51.8 and 89.1 points
(p<.001) respectively.
On the level of individual items, the most relevant and significant differences
(Effect Size) between the two groups were observed for using stairs both up
and down (more effort (1.4), more time (1.1)) and for walking small distances
in (1.1) and outdoors (1.5).


3 Relation between Risk Profile and Quality of Life

In Table 4 the significant correlations between risk profile and QoL are
shown for the entire study population. The severity of the risk profile was
significantly related to QoL on all the scales of the WSQ and on the physical
functioning and impairment of physical role domains of the RAND-36. There
was no significant correlation between risk profile and social functioning,
self-perceived health and the other domains of the RAND-36 or the Barthel
Index.

Table 4: Relation between Risk Profile and Quality of Life (Spearman's r)

RAND-36
Physical functioning -.66*
Physical role -.56*
WSQ
Using stairs -.64*
Walking indoors -.67*
Walking outdoors -.71*
Walking velocity -.63*

Only the significant correlations are shown, * p < .001

3.4 Discussion

This study addressed the interrelations between physical, social and
psychological dimensions of QoL in DM patients. The obvious physical
limitations of patients with DFUs, reflected by the WSQ and by the physical
functioning domain of the RAND-36, greatly affected QoL, and were
probably causing limitations in social functioning.
On an individual level, there were highly relevant and significant differences
for producing moderate and heavy physical effort, walking in and outdoors,
using the stairs both up and down (more effort, more time) and working
(lower production). In contrast with the results reported by Rijken3, we did
not find a relation between having a DFU and complaints of pain. Whereas
other studies found more psychological complaints in patients with foot


disease4, this was not found in our study for the item psychological
functioning. Very few of our patients had an acute phase of foot disease.
Perhaps they had learnt to accept their disabilities and had found a new
psychological balance.
In conclusion, an existing or previous ulcer has an obvious negative influence
on the physical and social aspects of quality of life in patients with diabetes
mellitus. This is in line with the findings of earlier studies 3,5.

In a general population of patients with diabetes, psychological and social
aspects contributed to the overall QoL, while physical complaints had less
influence 20. This suggests that having a diabetic foot changes the spectrum of
factors that influence QoL, with an increase in the impact of limitations
related to physical functioning and mobility.
The population studied is not very large and selected at a specific institution.
Therefore generalisation might be limited. However, the influence of physical
disabilities on quality of life, by decreasing mobility of patients, is very
significant and relevant for workers in the field of rehabilitation.
Despite the fact that the clinical situation was stable in all the patients with
DFUs at the time of the study, their mobility and physical functioning were
limited. The significant correlation between risk profile and QoL suggests
that the decrease in physical functioning and mobility in the patients with foot
disease was caused by physical restrictions due to the DFU itself, or due to
signs and symptoms of risk factors, such as neuropathy or angiopathy. This
decrease might have been further strengthened by restrictions imposed by
preventive patient education (for example patients are advised to walk only
short distances). Our data emphasize the necessity to pay attention to mobility
in patients with clinical stable foot ulcers.

In conclusion, diabetic foot ulcers have a large impact on quality of life,
especially on physical functioning, social functioning and mobility. Physical
disabilities, due to the presence of risk factors or ulcers, are responsible for
this decrease in quality of life.
In our opinion, combining diabetic foot prevention programmes with a
rehabilitation programme for patients with DFUs can increase quality of life.
Such a programme might provide physical training for these patients (to
enhance their condition and decrease disabilities), increase awareness about
adaptations and equipment to enhance mobility (prescription of special
footwear, walking aids or electric trikes and stair-lifts) and offer vocational
therapy.

This study was sponsored by a grant from the Vereniging Beatrixoord,
Haren, the Netherlands


3.5 References

1 Centraal Begeleidingsorgaan voor de Intercollegiale Toetsing,
Nederlandse Diabetes Federatie. Richtlijnen NDF/CBO de Diabetische
Voet. Heerenveen:Banda, 1998.
2 Palumbo PJ, Melton LJ. Peripheral vascular disease and diabetes. In:
Harris MI, Hamman RF eds. Diabetes in America. NIH publ. No. 85-
1468. Washington: US Government Printing Office, 1985; XV: 1-21.
3 Rijken PM, Dekker J, Dekker E et al. Clinical and functional correlates
of foot pain in diabetic patients. Disability and Rehabilitation 1998;
20(9): 330-36.
4 Carrington AL, Mawdsley SKV, Morley M, Kincey J, Boulton AJM.
Psychological status of diabetic people with or without lower limb
disability. Diabetes Research and Clinical Practice 1996; 32: 19-25.
5 Brod M. Quality of life issues in patients with diabetes and lower
extremity ulcers: patients and care givers. Quality of Life Research
1998; 7 (4): 365-72.
6 Fitzpatrick R, Fletcher A, Gore S, Jones D, Spiegelhalter D, Cox D.
Quality of life measures in health care: applications and issues in
assessment. British Medical Journal 1992; 305: 1074.
7 Revicki DA. Quality of life and non-insulin-dependent diabetes
mellitus. Diabetes spectrum 1990; 3: 260.
8 World Health Organisation. The first ten years of the World Health
Organisation. Geneva: WHO, 1959: 459.
9 Caputo JW, Cavanagh PR, Ulbrecht JS, Gibbons GW, Karchmer AW.
Assessment and management of foot disease in patients with diabetes
mellitus. New England Journal of Medicine 1994; 331: 854-60.
Leprosy Review 1986; 57: 261-67.
11 Uccioli L, Boulton AJM. Comparison of risk factors for foot problems
in diabetic patients attending hospital outpatient clinics in four
different European states. Diabet Med 1994; 11: 709-11.
12 Wagner FW. The dysvascular foot: a system for diagnosis and
treatment. Foot and Ankle 1981; 2: 64-122.
13 Zee K van der, Sanderman R. Het meten van de algemene
gezondheidstoestand met de RAND-36. Noordelijk Centrum voor
Gezondheidsvraagstukken, Rijksuniversiteit Groningen, 1993: 1-28.
14 Mahoney FI, Barthel DW. Functional evaluation: the Barthel Index.
Md State Med J 1965; 14: 61-65.
15 Wade DT, Collin C. The Barthel ADL Index: A standard measure of
physical disability? International Disability Studies 1988; 10: 64-67.


16 Roorda LD, Roebroeck ME, Lankhorst GJ, Tilburg TG van. De
vragenlijst loopvaardigheid: hierarchische schalen om beperkingen in
het opstaan en lopen te meten. Revalidata 1996; 18: 34-8.
17 Roorda LD, Roebroeck ME, Lankhorst GJ, Tilburg TG van.
Measuring functional limitations in rising and sitting down:
development of a questionnaire. Archives of Physical Medicine and
Rehabilitation 1996; 77: 663-69.
18 J.H.Zar , Biostatistical Analyses, 1999, New Jersey.
19 J.Cohen, Statistical Power Analysis for the Behavioral Scienes, New
York, 1969.
20 Rose M, Burkert U, Scholler G, Schirop T, Danzer G, Klapp BF.
Determinants of quality of life of patients with diabetes under
intensified insulin therapy. Diabetes Care 1998; 21(11): 1876-85.


Chapter 4

Symptom scoring systems to diagnose
distal polyneuropathy in diabetes:
the Diabetic Neuropathy Symptom score

J.W.G. Meijer, A.J. Smit, E. van Sonderen,
J.W. Groothoff, W.H. Eisma, T.P. Links

Diabetic Medicine, short version, in press.

© 2002 by Blackwell Ltd and Diabetes UK;
reprinted with their kind permission

Abstract

Aims Distal polyneuropathy (PNP) is the major risk factor for
diabetic foot disease. One of its diagnostic categories is
symptom scoring. Several scoring systems are available.
The generally accepted Neuropathy Symptom Score
(NSS) (17 items) is valid but extensive. We developed, on
expert opinion, the 4 item Diabetic Neuropathy Symptom
(DNS) score, very manageable but not yet validated. The
aim of this study was to validate the DNS-score for
diagnosing distal PNP in diabetes.
Methods In 73 patients, the score characteristics of the NSS and the
DNS-score were compared, and construct validity,
predictive value and reproducibility were assessed with
the Diabetic Neuropathy Examination score, Semmes
Weinstein Monofilaments and Vibration Perception
Threshold (clinical standards).
Results 43 men and 30 women were studied (mean duration of
diabetes 15 years (1-43), mean age 57 years (19-90)).
Twenty-four patients had type 1 diabetes, and 49 type 2.
Correlation between NSS and DNS-score was high
(Spearman r = 0.88). Patients scored more differentiated
on the DNS-score. The relation of the NSS and DNS-
score, respectively, with the clinical standards was good
(Spearman r = 0.21 - 0.60). Both scores had a comparable
predictive value. Reproducibility of the DNS-score was
good (Cohen weighted Kappa .78-.95). The DNS-score
was easier to perform and therefore preferred above the
NSS.
Conclusions The DNS-score is a validated symptom score, fast and
easy to perform in clinical practice, with high predictive
value to screen for PNP in diabetes.


4.1 Introduction

Distal symmetric polyneuropathy (PNP) is a very common complication of
diabetes and is considered to be a major causal factor in the majority of foot
ulcers in diabetic patients 1,2. To diagnose PNP, the San Antonio consensus
report advises that at least one measurement should be performed in 5
different diagnostic categories 3. One of these categories is symptom scoring.
In our opinion, the value of systematic assessment of symptoms is often
misunderstood in clinical practice, and is not based on standardised scoring of
a specific set of questions. Diagnosis is usually based on Quantitative
Sensory Testing or Physical Examination. However, symptoms are important
to evaluate, because they reflect the complaints of the patient, they may be of
additional diagnostic or prognostic value and treatment might be possible 4.
As diagnostic tests, symptom scores should fulfil the criteria as described by
Jaeschke et al. 5. The scores have to be validated (presence of an independent
reference standard, adequate spectrum and number of patients,
standardisation, soundly based item selection), they should be of predictive
value and manageable in clinical practice (reproducibility, performance in
clinical practice) 5.

Several scores have been developed to assess symptoms of diabetic
neuropathy.
The Neuropathy Symptom Score (NSS) 4, 6-8 and the Neuropathy Symptom
Profile (NSP) 9 both assess diabetic neuropathy. The NSS is the most widely
studied and accepted score, and known to be valid and sensitive 4, 6-8. The
Neuropathy Symptom Profile contains 34 test categories. It is validated and
can be read and scored by computer 9. Because both scores assess neuropathy
in general, they are rather extensive in clinical practice. The Michigan
Neuropathy Screening Instrument (MNSI) 10 and the modified NSS scores of
Veves and Young 11,12 have been developed specifically for distal diabetic
polyneuropathy. The MNSI is a combination of a symptom score (15 items)
and a physical examination score 10. The combination is valid and has a high
predictive value. However, there is no separate symptom score, as advised by
consensus reports 3. No information is available to review the modifications
of the NSS scores of Veves and Young 11,12. The Diabetes Symptom
Checklist type 2 (DSC-type 2) 13 and the McGill Pain Questionnaire 14 are
scores for diabetes in general and pain, respectively. The DSC-type 2 has
been validated both as an entire score and for neuropathy symptoms alone 13.
Of the items concerning neuropathy, only numbness and tingling sensations
at both hand and feet were associated with other diagnostic standards for
diabetic neuropathy 15. The McGill Pain Questionnaire scores for painful
diabetic leg problems 14, but no data is available about validity and predictive
value. The Diabetic Neuropathy Symptom score (DNS-score), developed at

Chapter 4: the DNS-score - 37

our hospital, consists of 4 items chosen on clinical relevance and experience,
as the most typical and clinically relevant for distal symmetric PNP in
diabetes. This score has not been validated or published before.

Because none of these scoring systems fulfil Jaeschke's criteria for diagnostic
tests 5, the aim of this study was to validate the DNS-score for diagnosing
distal symmetric PNP in diabetes, and to compare its score-characteristics
with the NSS.


Patients:
Our study group consisted of 73 patients with diabetes, covering the entire
spectrum of secondary complications. Informed consent was obtained from
all participating patients. Exclusion criteria were factors that may interfere
with the neurological condition of the subjects other than PNP.
Fifty of these 73 patients were randomly selected from the diabetes outpatient
clinic of the University Hospital Groningen. The other 23 patients, all known
with obvious diabetic foot complications or clinical neuropathy, were
selected from the Department of Diabetes at the Rehabilitation Centre Beat-
rixoord.
The characteristics of the 73 patients are shown in Table 1.

Table 1: Patient Characteristics

N 73
Mean age (years)(SD) 56.9 (16.1)
Min – max (years) 19 – 90
Mean duration DM (years) (SD) 14.9 (9.9)
Min – max (years) 1 – 43
Sex
Male – female 43 – 30
Type DM
1- 2 24 – 49
Mean HbA1c (%) (SD) 8.7 (1.4)
Min – max 6.6 – 13.5
Retinopathy 40%
Nephropathy 42%
Peripheral vascular disease 38%
Present or former ulcer 20%


Methods:
The same researcher (J.-W.G.M.) examined all 73 patients. First, the
symptom scores were performed followed by clinical standards; a physical
examination score ( the Diabetic Neuropathy Examination (DNE) score) and
quantitative sensory tests (Semmes Weinstein Monofilaments and vibration
perception thresholds), respectively.

1 Symptom Scores

1.1 NSS
The NSS consists of 17 items, 8 focusing on muscle weakness, 5 on sensory
disturbances and 4 on autonomic symptoms 4,6. Items that are answered
negative/absent are scored 0, presence scored as 1 point. Maximum score of
the NSS is 17 points 4, 6-8.

1.2 DNS-score
An expert panel of the University Hospital (Groningen, the Netherlands)
developed a 4 item symptom score for diabetic PNP. The panel consisted of a
diabetologist/endocrinologist, a specialist for internal vascular diseases, a
neurologist and a physician for rehabilitation medicine; all experienced in
diagnosing diabetic neuropathy. The DNS-score consists of the following
items: (1) unsteadiness in walking, (2) pain, burning or aching at legs or feet,
(3) prickling sensations at legs or feet, and (4) numbness at legs or feet.
Presence is scored as 1 point, absence as 0 points, maximum score 4 points.
Guidelines to use with the score are shown in Appendix 1.

2 Clinical Standards
The Diabetic Neuropathy Examination (DNE) score, Semmes-Weinstein
Monofilaments (SWMF) and Vibration Perception Threshold (VPT) were
chosen as clinical standards to study the construct validity of the symptom
scoring systems for PNP.

2.1 DNE-score
The DNE-score is a validated, hierarchical physical examination score to
diagnose distal symmetric PNP in diabetes 16. It exists of 8 items; 2 items
testing muscle strength, 1 item testing a tendon reflex and 5 items testing
sensation. The maximum score is 16 points. A score of > 3 points is defined
as disturbed/abnormal.

2.2 Semmes-Weinstein Monofilaments (SWMF)
SWMF's were tested on the plantar surface of the hallux and central at the
heel (when necessary after removal of excessive callus). This method was
performed standardised according to generally accepted guidelines 17-20. The


"yes-no" method was used. This means that the patient says yes each time
that he or she senses the application of a monofilament. Six trials were taken,
when the patient was unable to respond correct in more than 1 trial, a heavier
monofilament was taken. The 1, 10 and 75 gram monofilaments have been
used 17-20. This resulted in four categories: category 1: 1 gram monofilament
felt; category 2: 10 gram felt, 1 gram not felt; category 3: 75 gram felt, 10
gram not felt; category 4: 75 gram not felt. In categories 1 and 2 sensitivity is
present, therefore they are scored as normal. Categories 3 and 4 are scored as
abnormal.

2.3 Vibration Perception Threshold (VPT)
VPTs were determined using a hand-held biothesiometer (Biomedical Instru-
ments Inc., Ohio, USA). VPT was tested at the dorsum of the hallux on the
interphalangeal joint and at the lateral malleolus. It was performed in a
standardised way 21-23. The voltage of vibration was increased until the patient
could perceive a vibration. This was done three times. The mean of these
three was used to determine the VPT. Age-adjusted reference values were
used 21-23. Values higher than the mean+2*SD (reference value) were
considered as abnormal.

Reproducibility
In order to test reproducibility of the DNS-score, inter- and intrarater
agreement were assessed in a separate study on 10 patients. The 6 women
and 4 men, with a mean age of 50.0 years (SD15.9) had a wide range of
neuropathy severity. The mean duration of DM was 11.5 years (SD 10.5); 3
participants had type 1 DM and 7 had type 2 DM. Two doctors, an
endocrinologist and a physician for rehabilitation medicine, both experienced
in diagnosing diabetic neuropathies, rated these patients twice with an
interval of one week.

Statistical Analyses
Internal consistency of the symptom scores was assessed by calculating
Cronbach's alpha, and reliability coefficient Rho, which is comparable to
alpha. The statistical package SPSS-PC was used to compute the descriptive
statistics, reliability coefficient Crohnbach’s alpha, Spearman's correlation
coefficient r, Student's t-test and ROC curves 24. Inter- and intrarater
agreement was assessed using Cohen’s weighted Kappa 25,26.


4.3 Results

In Table 2 general information about the NSS and the DNS-score is shown.
The reliability of the DNS-score seems to be a little lower than of the NSS.
This is, however, due to the considerable reduction of items, and not to a
lower association between the items. Correlation (Spearman r) between these
two symptom scores is, as expected, high: .88.

Table 2: Characteristics of the symptom scores.

NSS DNS-score
Mean (SD) 1.9 (2.0) 1.1 (1.3)
Reliability (alpha) .74 .64
Number of items 17 4
Maximum score 10 4
Non used items 4 0

Relationship of the NSS and DNS-score with the Clinical Standards
Spearman's correlation coefficient r for the DNE-score with the NSS and
DNS-score was similar with values of .56 and .60 (both p<.001),
respectively. Spearman's correlation coefficient r for the SWMF with the
NSS and DNS-score was .21 (not significant) and .25 (p<.05), respectively.
For VPT, Spearman's correlation coefficient r with the NSS and DNS-score
was .46 and .56 (both p<.001), respectively.
The NSS and the DNS-score predicted the results of the clinical standards
adequately, as shown in Table 3.


Table 3 Relation Clinical Standards - Symptom Scores

group 0= normal on clinical standard, group 1= disturbed on clinical standard

DNE-score:
N mean NSS (SD) mean DNS (SD)
0 24 .92 (1.47) .42 (.93)
1 48 2.42 (2.07) 1.52 (1.24)
p .002 p .000

Semmes Weinstein Monofilaments Hallux:
0 45 1.42 (1.42) .84 (1.04)
1 25 2.64 (2.63) 1.56 (1.41)
p .014 p .019

Vibration Perception Threshold Hallux:
0 39 1.28 (1.47) .67 (.98)
1 32 2.63 (2.34) 1.69 (1.30)
p .004 p .000

Sensitivity / Specificity

Figure 1 shows the ROC-curves of, respectively, the NSS and DNS-score as
compared with the DNE-score. For NSS and DNS-score the areas under the
curve are .75 and .78, respectively. Using the SWMF at the hallux these
values are .62 and .65, respectively; and using VPT .68 and .73, respectively.
At a cut off point of 0 versus 1-4 for the DNS-score, sensitivity was 79% and
specificity 78% regarding the DNE-score. Regarding SWMF sensitivity was
81% and specificity 56%, for VPT sensitivity was 81% and specificity 58%.


Figure 1: ROC-curves of NSS and DNS-score, respectively, in relation to the
DNE-score.

1,00

,75

,50

sensitivity

,25

Referenc e Li
DNS -score
0,00
NSS
0,00 ,25 ,50 ,75 1,00

1-specificity

Reproducibility of the DNS-score

The intrarater agreement showed Cohen’s weighted Kappa’s for both raters
of .89 and .78, the interrater agreement on two occasions was .95, and .83,
respectively, indicating a good to very good level of agreement 25,26.


4.4 Discussion

The NSS is a validated and widely accepted symptom score for diabetic
neuropathy 4, 6-8. The most frequent form of neuropathy in diabetes and major
risk factor for diabetic foot disease is distal symmetric PNP 1. Several items
of the NSS are seldom scored, because the NSS has not been developed
specifically for distal PNP. Large groups of diabetic patients need to be
screened regularly to diagnose PNP early as part of prevention of diabetic
foot ulcers. Consequently, several other scoring systems and modifications
have been developed, but they do not sufficiently fulfil all the criteria
necessary for adequate diagnostic tests. In this study, the DNS-score was
validated with the aim of achieving a manageable symptom scoring system
for diagnosing distal symmetric diabetic PNP in clinical practice and
epidemiological studies.

We compared the score-characteristics of the DNS-score with the original
NSS. Furthermore, the construct validity of the NSS and DNS-score has been
studied by comparing the scores with the clinical standards chosen: the DNE-
score, SWMF and VPT. We conclude that both symptom scores adequately
fulfil the criteria for diagnostic tests, as mentioned in the introduction. We
prefer the DNS-score for further use as symptom score, because the
differences between the scores on validity and predictive value are small and
not clinically relevant, and the manageability of the DNS-score is excellent.
Consisting of only 4 items, the DNS-score is fast and easy to perform in
clinical practice with a high reproducibility.

Diagnostic tests can be discriminative (diagnosis), predictive (prognosis) or
evaluative (follow up). The DNS-score is validated with clinical standards on
discriminative and predictive values. For evaluation of treatment or follow
up, the score might be too short with only four items. However, in the NSS
the number of items related to PNP is also very limited.
Unfortunately the exact weight of the different categories, individual or in
combination, in diagnosing diabetic PNP and predicting diabetic foot
complications, is not yet known.

Sensitivity and specificity of the DNS-score were high regarding the DNE
score, SWMF and VPT. Because the DNS-score will be used for screening
purposes, sensitivity is preferred above specificity. A score of 1 or more
points on the DNS-score is very sensitive for presence of diabetic PNP. In
combination with the results of the other diagnostic categories of the San
Antonio Consensus, this gives an indication of type and severity of PNP.


Controversy exists about the use of symptom scoring in diagnosing PNP in
diabetes. Because symptoms of neuropathy (pain, numbness and tingling) are
present in 30-40% of all people with diabetes, Mayfield et al. concluded that
the presence or absence of symptoms should not be used to assess the risk of
ulcers or amputation 27. Valk et al. found that symptoms of neuropathic pain
and paraesthesia were neither correlated with the results of physical
examination nor with the results of neurophysiological examination 15. In
another study they concluded that only symptoms of numbness and tingling
sensations in hand and feet (items of the DSC-type 2), were associated with
the clinical examination, but not with neurophysiological examination 28.
Franse et al. studied whether a patient history could replace the Clinical
Neurological Examination (CNE). The individual symptoms were
insufficiently predictive for the presence of polyneuropathy. They concluded
that individual symptoms could not replace the CNE 29. Dyck et al. found an
association between complaints of diabetic neuropathy, abnormalities of the
clinical examination and abnormalities of nerve conduction 7. In our report
significant and clinically relevant correlations have been shown between the
symptom scores and the DNE-score, SWMF and VPT, respectively; which
are all accepted tests with known predictive value for diabetic foot
complications. Therefore, as the consensus advises, we state that symptom
scoring deserves to be a part of the diagnostic set, complementary to other
diagnostic categories for diabetic PNP 3.
It is known that the reliability of symptom scores may be poorer than the
reliability of the other diagnostic categories 3,4,8. This might be caused by the
subjectivity of the scores, leading to a poor reproducibility. The consensus
advises to score dichotomous to enhance reliability 3. In the DNS-score, a
short and dichotomous symptom score, the reproducibility is high.

In conclusion, the DNS-score, a symptom score specific for distal symmetric
PNP in diabetes, has now been validated, and is fast and easy to perform in
clinical practice. As the consensus advises, this scale has to be used
complementary to other diagnostic categories as for example standardised
physical examination (for example the DNE-score) and quantitative sensory
testing. Further prospective studies are necessary with the DNS-score, the
DNE-score and other diagnostic tests, to assess the predictive value of the
scales and items.


4.5 References

overview. Diabet Med 1996; 13: s12-s16.
2 Caputo GM, Cavanagh PR, Ulbrecht JS, Gibbons GW, Karchmer AW.
Assessment and management of foot disease in patients with diabetes.
N Engl J Med 1994; 331: 854-860.
3 Consensus Statement: Report and recommendations of the San Anto-
nio conference on diabetic neuropathy. Diabetes Care 1988; 11: 592-
97.
4 Dyck PJ. Detection, characterization and staging of polyneuropathy:
assessed in diabetics. Muscle and Nerve 1988; 11: 21-32.
5 Jaeschke R, Guyatt G, Sacket DL. Users' guides to the medical
literature: how to use an article about a diagnostic test. JAMA 1994;
271: 389-391.
6 Dyck PJ, Sherman WR, Hallcher LM Service FJ, O'Brien PC, Grina
LA, Palumbo PJ, Swanson CJ. Human diabetic endoneurial sorbitol,
fructose and myo-inositol related to sural nerve morphometry. Annals
of Neurology 1980; 6: 590-96.
7 Dyck PJ, Karnes JL, Daube J, O'Brien P, Service JF. Clinical and
neuropathological criteria for the diagnosis and staging of diabetic
polyneuropathy. Brain 1985; 108: 861-80.
8 Dyck PJ, Kratz KM, Lehman KA, Karnes JL, Melton LJ, O'Brien PC,
Litchy WJ, Windebank AJ, Smith BE, Low PA, Service FJ, Rizza RA,
Zimmerman BR. The Rochester diabetic neuropathy study: design,
criteria for types of neuropathy, selection bias, and reproducibility of
neuropathic tests. Neurology 1991; 41: 799-807.
9 Dyck PJ, Karnes J, O'Brien PC, Swanson CJ. Neuropathy Symptom
Profile in health, motor neuron disease, diabetic neuropathy, and
amyloidosis. Neurology 1986; 36: 1300-08.
10 Feldman EL, Stevens MJ, Thomas PK, Brown MB, Canal N, Greene
DA. Practical two-step quantitative clinical and electrophysiological
assessment for the diagnosis and staging of diabetic neuropathy.
Diabetes Care 1994; 17: 1281-89.
11 Veves A, Manes C, Murray HJ, Young MJ, Boulton AJM. Painful
neuropathy and foot ulceration in diabetic patients. Diabetes Care
1993; 16: 1187-89.
12 Young MJ, Boulton AJM, Macleod AF, Williams DRR, Sonksen PH.
A multicentre study of the prevalence of diabetic peripheral
neuropathy in the United Kingdom hospital clinic population.
Diabetologia 1993; 36: 150-54.


13 Grootenhuis PA, Snoek FJ, Heine RJ, Bouter LM. Development of a
type 2 diabetes symptom checklist: a measure of symptom severity.
Diabet Med 1994; 11: 253-61.
14 Masson EA, Hunt L, Gem JM, Boulton AJM. A novel approach to the
diagnosis and assessment of symptomatic diabetic neuropathy. Pain
1989; 38: 25-28.
15 Valk GD, Grootenhuis PA, Bouter LM, Bertelsmann FW. Complaints
of neuropathy related to the clinical and neurophysiological assessment
of nerve function in patients with diabetes mellitus. Diab Res and Clin
Pract 1994; 26: 29-34.
16 Meijer JWG, van Sonderen E, Blaauwwiekel EE, Smit AJ, Groothoff
JW, Eisma WH, Links TP. Diabetic neuropathy Examination: a
hierarchical scoring system to diagnose distal polyneuropathy in
diabetes. Diabetes Care 2000; 23: 750-53.
Leprosy Review 1986; 57: 261-67.
18 Kumar S, Fernando DJS, Veves A, Knowles EA, Young MJ, Boulton
AJM. Semmes Weinstein Monofilaments: a simple, effective and inex-
pensive screening device for identifying diabetic patients at risk of foot
ulceration. Diab Res and Clin Pract 1991; 13: 63-68.
19 Mueller MJ. Identifying patients with diabetes mellitus who are at risk
for lower extremity complications: use of Semmes Weinstein
monofilaments. Physical Therapy 1996; 76: 68-71.
20 Armstrong DG, Lavery LA, Vela SA, Quebedeaux TL, Fleischli JG.
Choosing a practical screening instrument to identify patients at risk
for diabetic foot ulceration. Archives of Internal Medicine 1998; 158:
289-92.
21 Goldberg JM, Lindblom U. Standardised method of determining
vibratory perception thresholds for diagnosis and screening in
neurological investigation. J of Neur, Neurosurg and Psych 1979; 42:
793-803.
22 Bloom S, Till S, Sonksen P, Smith S. Use of a biothesiometer to
measure individual vibration thresholds and their variation in 519 non-
diabetic subjects. BMJ 1984; 288: 1793-95.
23 Young MJ, Breddy L, Veves A, Boulton AJM. The prediction of
diabetic neuropathic foot ulceration using vibratory perception
thresholds. Diabetes Care 1994; 17: 557-60.
24 Hanley JA, McNeil BJ. A method of comparing the areas under the
receiver operating characteristic curves derived from the same cases.
Radiology 1983; 148: 839-43.
25 Landis JR, Koch GG. The measurement of observer agreement for
categorical data. Biometrics 1977; 33: 159-74.


26 Altman DG, ed. Practical statistics for medical research. London:
Chapman and Hall, 1997.
27 Mayfield JA, Reiber GE, Sanders LJ, Janisse D, Pogach LM.
Preventive foot care in people with diabetes. Diabetes Care 1998; 21:
2161-77.
28 Valk GD, Nauta JJP, Strijers RLM, Bertelsman FW. Clinical
examination versus neurophysiological examination in the diagnosis of
diabetic polyneuropathy. Diabet Med 1992; 9: 716-21.
29 Franse LV, Valk GD, Dekker JH, Heine RJ, van Eijk JTM. Numbness
of the feet is a poor indicator for polyneuropathy in type 2 diabetic
patients. Diabet Med 2000; 17: 105-10.


Appendix 1: DNS-score

DNS-score and guidelines

1 Are you suffering of unsteadiness in walking?
need for visual control, increase in the dark, walk like a drunk man,
lack of contact with floor
remark: it is assumed that the patient has no limiting visual, hearing or
central neurological deficits.

2 Do you have a burning, aching pain or tenderness at your legs or
feet?
remark: it is assumed that intermittent claudication has been made
unlikely by excluding pain which develops during walking and
disappears upon halting, and that ischaemic rest pain is made unlikely
by lack of effect of dependency, in both cases further supported by the
lack of absent foot-ankle pulsation and/or reduced ankle- and toe
pressures.

3 Do you have prickling sensations at your legs and feet?
occurring at rest or at night, distal>proximal, stocking glove
distribution

4 Do you have places of numbness on your legs or feet?
Distal>proximal, stocking glove distribution

The questions should be answered "yes" (positive: 1 point) if a symptom occurred more
times a week during the last 2 weeks or "no" (negative: no point) if it did not.
Max. score: 4 points
0 points: PNP absent
1-4 points: PNP present


Chapter 5

Diabetic Neuropathy Examination:
a hierarchical scoring system to diagnose
distal polyneuropathy in diabetes

J.W.G. Meijer, E. van Sonderen, E.E. Blaauwwiekel,
A.J. Smit, J.W. Groothoff, W.H. Eisma, T.P. Links

Diabetes Care 2000; 23 (6): 750-753.

© 2000 by the American Diabetes Association;
reprinted with their kind permission

Abstract

Objective Existing physical examination scoring systems for distal
diabetic polyneuropathy (PNP) do not fulfil all of the
following criteria: validity, manageability, predictive
value, and hierarchy. The aim of this study was to adapt
the Neuropathy Disability Score (NDS) to diagnose PNP
in diabetes mellitus (DM) so that it fulfils these criteria.
Methods A total of 73 patients with DM were examined with the
NDS. Monofilaments and biothesiometry were used as
clinical standards for PNP to modify the NDS.
Results A total of 43 men and 30 women were studied; the mean
duration of DM was 15 years (1-43), and the mean age
was 57 years (19-90). Twenty-four patients had DM type
1 and 49 had type 2 DM. Clinically relevant items were
selected from the original 35 NDS items (specific item
scored positive score in > 3 patients). The resulting 8-item
Diabetic Neuropathy Examination score (DNE) could
accurately predict the results of the clinical standards and
is strongly hierarchical (H-value 0.53). The sensitivity and
specificity of the DNE at a cut-off level of 3 to 4 were
0.96 and 0.51 for abnormal monofilament scores,
respectively. For abnormal biothesiometry scores, these
values were 0.97 and 0.59, respectively. Reproducibility,
as assessed by inter- and intrarater agreement, was good.
Conclusions The DNE is a sensitive and well-validated hierarchic
scoring system that is fast and easy to perform in clinical
practice.


5.1 Introduction

Early detection of symmetric distal sensori-motor polyneuropathy (PNP) is
important in patients with diabetes mellitus (DM), because preventive inter-
ventions can be applied to decrease morbidity 1. Unfortunately, no "gold
standard" exists for diagnosing PNP, but a consensus panel has recommended
that at least 1 measurement should be performed in 5 different diagnostic
categories. One of these categories is a standardised physical examination 2,3.
In our opinion, diagnostic tests should fulfil the following criteria: validation
(presence of independent reference standard, adequate spectrum and number
of patients, standardisation, soundly based item selection), predictive value,
manageability (reproducibility, performance in clinical practice) and
hierarchy. Frequently used and accepted examination scores for diabetic
neuropathy are the Neuropathy Disability Score (NDS) 4, the Neuropathy
Impairment Score in the Lower Limbs (NIS-LL) 5,6, various modified NDS
scores 7,8, the Neuropathy Deficit Score 9, the Michigan Neuropathy
Screening Instrument (MNSI) 10 and the Clinical Examination score of Valk
(CE-V) 11.

The NDS was designed for neuropathy in general 4. Although the score is
well founded and complete, it is difficult to perform in clinical practice on
patients with diabetic foot problems. Precise descriptions of how the tests
should be performed and how items should be scored are lacking. The NIS-
LL is a modification of the NDS specific for distal PNP, although motor
activity grading is the focus and involves 64 of a maximum of 88 points 5,6.
The NIS-LL has not been validated. Various other modified NDS scoring
systems have been used, such as those of Veves et al. 7 and Young et al. 8.
However, these instruments also have not been validated and no information
is available on their predictive value regarding the results of clinical
standards. The Neuropathy Deficit Score is a neurological examination score
aimed at anatomical levels in the legs and arms 9. It has not been validated
and no information is available about how to interpret modifications, which is
also the case for the other modified NDS scoring systems 7,8. Feldman et al. 10
developed a combination of two scoring systems: the Michigan Neuropathy
Screening Instrument (symptom and examination score) and the Michigan
Diabetic Neuropathy Score (neurological examination and nerve conduction
studies). These scores do not have a separate examination score, as advised
by consensus reports 2,3. The CE-V can be used to examine sensory functions,
tendon reflexes and muscle strength in the lower extremities 11. The scoring
systems of Feldman et al. and Valk et al. have been validated and are easy to
perform in clinical practice. None of the afore mentioned scores is known to
be hierarchical.

Chapter 5: the DNE-score - 53

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