epidemiology of diabetic foot problems and predictive factors for.pdf
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Epidemiology of diabetic foot problems and predictive factors for
limb loss
Aziz Nathera,4, Chionh Siok Beeb, Chan Yiong Huakc, Jocelyn L.L. Chewa, Clarabelle B. Lina,Shuhui Neoa, Eileen Y. Sima
aDepartment of Orthopaedic Surgery, National University Hospital, Singapore
bDivision of Endocrinology, Department of Medicine, National University Hospital, Singapore
cBiostatistics Unit, Yong Loo Lin School of Medicine, National University of Singapore, Singapore
Received 8 August 2006; received in revised form 28 March 2007; accepted 23 April 2007
Abstract
Objectives: The aim of this study was to evaluate the epidemiology of diabetic foot problems (DFP) and predictive factors for major
amputations (below- and above-knee). Methods: This is a prospective study of 202 patients treated in National University Hospital (NUH)
during the period of January 2005 to May 2006. A protocol was designed for documentation including patient profile, type of DFP, presence
of risk factors, comorbidities and complications, clinical presentation, investigations, treatment given, and final outcome. The predictors for
limb loss were determined using univariate and stepwise logistic regression analysis. Results: One hundred ninety-two patients had Type 2
diabetes. Mean age of cohort was 60 years, with male to female ratio of 1:1. Incidence of DFP was significantly higher in Malays ( P=.0015)
and Indians (P=.036) and significantly lower in Chinese (Pb.05). Of patients, 72.8% had poor endocrine control (GHb level N7%), and
42.1% of patients had sensory neuropathy based on 5.07 SemmesWeinstein Monofilament test. Common DFP included gangrene (31.7%),
infection (abscess, osteomyelitis) (28.7%), ulcer (27.7%), cellulitis (6.4%), necrotizing fasciitis (3.5%) and Charcots osteoarthropathy
(2.0%). Surgery was performed in 74.8% of patients and major amputation in 27.2% of patients (below-knee in 20.3% and above-knee in
6.9%). Conclusions: This is the first detailed prospective study evaluating predictive factors for major amputations in patients with DFP.
Significant univariate predictive factors for limb loss were age above 60 years, stroke, ischaemic heart disease, nephropathy, peripheral
vascular disease (PVD), sensory neuropathy, glycosylated haemoglobin level, Ankle Brachial Index (ABI) b0.8, gangrene, infection, and
pathogens such as methicillin-resistant Streptococcus aureus (MRSA) and Staphylococcus aereus. Upon stepwise logistic regression
analysis, only PVD and infection were significant.
D 2008 Elsevier Inc. All rights reserved.
Keywords:Diabetes; Amputation; Risk factors; Epidemiology
1. Introduction
The prevalence of diabetes in Singapore is 8.2% in 2004(Ministry of Health Singapore, 2004). Diabetic foot prob-
lems (DFP) are very common in Singapore, accounting for
approximately one fifth of all emergency admissions in
National University Hospital (NUH). Every year, almost
700 lower limb amputations resulting from diabetic foot
complications are performed (Ministry of Health Singapore,
1993). According to Ministry of Health, Singapore, guide-lines (Ministry of Health Singapore, 1999), the comprehen-
sive care of a patient with diabetes mellitus included good
endocrine control, education on endocrine control, quarterly
monitoring of glycosylated haemoglobin (GHb) levels,
yearly eye checkups, and yearly foot screening. With better
knowledge of the various predictive factors that determine
limb loss (Fejfarova, Jirkovska, Skibova, & Petkov, 2002;
Gurlek, Bayraktar, Savas, & Gedik, 1998; Hamalainen,
Ronnemaa, Halonen, & Toikka, 1999; Hennis, Fraser,
1056-8727/08/$ see front matterD 2008 Elsevier Inc. All rights reserved.
doi:10.1016/j.jdiacomp.2007.04.004
4 Corresponding author. Department of Orthopaedic Surgery, Yong
Loo Lin School of Medicine, National University of Singapore, Singapore.
Tel.: +65 6772 4323; fax: +65 6778 0720.
E-mail address: [email protected] (A. Nather).
Journal of Diabetes and Its Complications 22 (2008) 7782
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Jonnalagadda, Fuller, & Chaturvedi, 2004; Imran, Ali, &
Mahboob, 2006; Lehto, Ronnemaa, Pyorala, & Laakso,
1996; Leung, Ho, Carnett, Lam, & Wong, 2001; Miyajima,
Shirai, Yamamoto, Okada, & Matsushita, 2006; Nelson
et al., 1988; Resnick et al., 2004; Selby & Zhang, 1995;
Sheahan et al., 2005; Tseng, 2006; Young, Maynard, Reiber,
& Boyko, 2003), the number of cases of lower limbamputations could be reduced.
2. Research designs and methods
This is a prospective study of 202 patients treated in
NUH Multi-Disciplinary Team for DFP during the period
January 2005 to May 2006. A special protocol which was
designed for documentation included patient profileage,
sex, and marital status; duration and type of diabetes;
presence of risk factors such as smoking, alcoholism,
obesity, and hyperlipidaemia; presence of complications
including retinopathy, nephropathy, and peripheral vascular
disease (PVD); and presence of comorbidities such as
hypertension, ischaemic heart disease (IHD), and stroke.
Other information documented included the types of DFP,
namely, gangrene, infection (abscess, osteomyelitis), ulcer,
cellulitis, necrotizing fasciitis and Charcots osteoarthrop-
athy. The ulcers were graded according to Wagners
Classification (Pendsey, 2003) (Grade 0: high-risk foot;
Grade 1: superficial ulcer; Grade 2: deep ulcer penetrating
to tendon, bone, or joint; Grade 3: deep ulcer with abscess
or osteomyelitis; Grade 4: localized gangrene; Grade 5:
extensive gangrene requiring a major amputation) as well
as neuropathy as indicated by the 5.07 SemmesWeinsteinMonofilament Test. Investigations recorded also included
full blood count, erythrocyte sedimentation rate, C-reactive
protein, GHb levels, urea and electrolytes, and blood and
wound cultures. In addition, the treatment given (the type
of primary surgery performed or conservative treatment
instituted) and the final outcome of treatment (limb saved
or limb lost) were studied.
All patients were reviewed weekly in the first month
followed by monthly reviews.
Photographs of patients feet with DFP were taken for
better documentation. DFP were classified according to
Kings Classification (Edmonds & Foster, 2005) (Stage 1:normal; Stage 2: high-risk; Stage 3: ulcerated; Stage 4:
cellulitic; Stage 5: necrotic; Stage 6: major amputation).
Patients who underwent distal operations such as ray
amputation, desloughing, incision and drainage (I&D), or
toe disarticulation were said to have their limbs saved, while
patients who underwent major operations such as below-
knee amputation (BKA) or above-knee amputation (AKA)
were said to have their limbs lost.
All statistical analysis were performed using SPSS 14.0
with statistical significance set atPb.05. Predictors for limb
loss were determined using univariate and stepwise logistic
regression analysis.
3. Results
The age of patients ranged from 21 to 91 years, with
mean age being 60.0 years. Majority of patients were in
their fifth and sixth decades. Bose (1978) also found the
average age to be about 60 years. The ratio of males to
females was 1:1, although Bose found the ratio of males tofemales to be 1:1.5. Racial distribution was 45.5% Chinese,
32.7% Malays, 17.8% Indians, and 4.0% other races. When
compared against the racial distribution of Singapores
national population (Singapore Department of Statistics,
2000), incidence of DFP in our cohort was significantly
higher in Malays (P=.0015) and Indians (P=.036) and
significantly lower in Chinese (Pb.05). Previous studies on
diabetic foot lesions in Singapore (Bose, 1979; Bose, 1978;
Cheah et al., 1985; Lee & Bose, 1985) did not study the
incidence of DFP amongst the different races.
One hundred ninety-two patients had Type 2 diabetes,
and 10 had Type 1. Duration of diabetes ranged from 1 to
48 years. Of patients, 41.6% had diabetes between 1 and
10 years duration, 39.1% between 11 and 20 years, 14.3%
between 21 and 30 years, and 5.0% with more than
30 years duration.
Majority of patients (72.8%) had poor control of
diabetes, as indicated by their GHb levels (N7%).
The most common comorbidities were hypertension
(74.8%), followed by IHD (36.1%) and stroke (8.9%). Risk
factors included smoking (19.3%), alcoholism (9.4%),
obesity (8.4%), and hyperlipidaemia (51.0%). With respect
to the complications of diabetes, 44.1% of patients had
retinopathy, and 51.5% had nephropathy.
The most common DFP were gangrene (31.7%),infection (abscess and osteomyelitis) (28.7%), and ulcer
(27.7%). Others included cellulitis (6.4%), necrotizing
fasciitis (3.5%), and Charcots osteoarthropathy (2.0%).
Ulcers encountered were Grade 1 in 15 patients, Grade 2 in
27, and Grade 3 in 14.
Infections were encountered in 122 patients (60.4%)
63 patients (31.2%) with monomicrobial infections and
59 patients (29.2%) with polymicrobial infections. This is
based on blood cultures performed for all patients and
swabs for culture in patients with ulcer or discharge. In
patients undergoing operation, tissue from the infected area
was sent for culture. This is rather different to an earlierstudy performed by Bose (Bose, 1979), who found
monomicrobial infections in 53.3% and polymicrobial
infections in 46.7%. The commonest pathogens encoun-
tered in the group with monomicrobial infections were
Staphylococcus aureus (34.9%), Pseudomonas aeruginosa
(17.5%), Streptococcus agalactiae Group B (11.1%), and
methicillin-resistant Streptococcus au reu s (MRSA)
(11.1%). In comparison,Bose (1979)found monomicrobial
infections to consist of Streptococcus aureus (30%),
P. aeruginosa (30%), Proteus (22.5%) and Klebsiella
(17.5%). Fifty-nine patients had polymicrobial infec-
tions, and the commonest pathogens encountered were
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Table 1
Results of evaluation of factors as predictive factors of limb loss
Risk factor
Limb loss Unadjusted Stepwise analysis
Positive Negative OR (95% CI) Pvalue OR (95% CI) Pvalue
Age
V60 years 19 (18.4) 84 (81.6) 1.0
N60 years 36 (36.4) 63 (63.6) 2.5 (1.34.8) .005
Gender
Male 26 (25.2) 77 (74.8) 1.0
Female 29 (29.3) 70 (70.7) 1.2 (0.72.3) .518
Race
Chinese 25 (27.2) 67 (72.8) 1.0
Malay 15 (22.7) 51 (77.3) 0.8 (0.41.6) .527
Indian 12 (33.3) 24 (66.7) 1.3 (0.63.1) .490
Others 3 (37.5) 5 (62.5) 1.6 (0.47.2) .536
Comorbidities
Hypertension Yes 43 (28.5) 108 (71.5) 1.3 (0.62.7) .493
No 12 (23.5) 39 (76.5) 1.0
IHD Yes 28 (38.4) 45 (61.6) 2.4 (1.24.4) .008No 27 (20.9) 102 (79.1) 1.0
Stroke Yes 9 (50.0) 9 (50.0) 3.0 (1.18.0) .028
No 46 (25.0) 138 (75.0) 1.0
Risk factors
Alcoholism Yes 3 (15.8) 16 (84.2) 0.5 (0.11.7) .249
No 52 (28.4) 131 (71.6) 1.0
Obesity Yes 3 (17.6) 14 (82.4) 0.5 (0.22.0) .360
No 52 (28.1) 133 (71.9) 1.0
Smoking Yes 12 (30.8) 27 (69.2) 1.2 (0.62.7) .581
No 43 (26.4) 120 (73.6) 1.0
Hyperlipidaemia Yes 33 (32.0) 70 (68.0) 1.7 (0.93.1) .119
No 22 (22.2) 77 (77.8) 1.0
ComplicationsRetinopathy Yes 24 (27.0) 65 (73.0) 1.0 (0.51.8) .941
No 31 (27.4) 82 (72.6) 1.0
Nephropathy Yes 40 (38.5) 64 (61.5) 3.5 (1.86.8) b.001
No 15 (15.3) 83 (84.7) 1.0
PVD Yes 45 (48.4) 48 (51.6) 9.3 (4.320.0) b.001 8.4 (3.918.3) b.001
No 10 (9.2) 99 (90.8) 1.0
Sensory neuropathy Yes 30 (35.3) 55 (64.7) 2.0 (1.13.8) .029
No 25 (21.4) 92 (78.6) 1.0
ABI b0.8 Yes 40 (36.7) 69 (63.3) 3.0 (1.55.9) .001
No 15 (16.1) 78 (83.9) 1.0
Type of DFP
Gangrene 30 (46.9) 34 (53.1) 4.0 (2.17.7) b.001
Infection 6 (10.3) 52 (89.7) 0.2 (0.10.6) .001 0.3 (0.10.7) .011
Ulcer 15 (26.8) 41 (73.2) 1.0 (0.51.9) .930Cellulitis 0 (0.0) 13 (100.0) N.A .999
Necrotizing fasciitis 4 (57.1) 3 (42.9) 3.8 (0.817.4) .090
Charcots osteoarthropathy 0 (0.0) 4 (100.0) N.A .999
Diabetes mellitus type
Type 1 2 (20.0) 8 (80.0) 1.0
Type 2 53 (27.6) 139 (72.4) 1.5 (0.37.4) .601
Duration of diabetes
N30 years 2 (20.0) 8 (80.0) 1.0
110 years 21 (25.0) 63 (75.0) 1.3 (0.36.8) .729
1120 years 21 (26.6) 58 (73.4) 1.4 (0.37.4) .656
(continued on next page )
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Staphylococcus aureus (39.0%), P. aeruginosa (35.6%),
Bacteroides fragilis (23.7%), and Streptococcus agalactiae
Group B (20.7%). Bose did not describe the distribution of
flora found with his polymicrobial infections. When both
monomicrobial and polymicrobial infections were consid-
ered together as one entity, the commonest pathogens
encountered were Staphylococcus aureus (22.3%), P.
aeruginosa (15.8%), and B. fragilis (9.9%).
Of patients, 42.1% were found to have sensory neuro-
pathy based on the 5.07 SemmesWeinstein monofilament
test. With regard to the ABI measurements, 54.2% had ABI
b0.8 (indicating ischaemia).
Of patients, 74.8% underwent surgical treatment. The
most common operations performed were desloughing
(29.7%) and ray amputation (18.8%). Other procedures
included I&D (11.9%), toe disarticulation (1.5%), and split
skin grafting (1.5%). Conservative treatment was instituted
in 25.2% of patients.Limb loss occurred in 27.2% of patients20.3% due to
BKA and 6.9% due to AKAsignificantly lower than the
higher amputation rate of 40% found by Bose (1978), with
120 major amputations performed out of a total of 300
diabetic gangrene cases.
3.1. Predictive factors for limb loss
Table 1 shows the results of our study for evaluating
various factors as predictive factors for limb loss. None of
the previous work on DFP performed in Singapore (Bose,
1979; Bose, 1978; Cheah et al., 1985; Lee & Bose, 1985)studied predictive factors for limb salvage in patients with
DFP. This article is a detailed analysis of DFP in our local
population studying not only the epidemiology of DFP, its
clinical presentation, and investigations but also the evalua-
tion of possible predictive factors for limb loss.
3.1.1. Age
Patients aged above 60 years was found to be a
significant predictive factor for limb loss in our study
(P=.005), similar to findings by Leung et al. (2001).
However, Gurlek et al. (1998) and Nelson et al. (1988)
found age not to be significant in their studies.
3.1.2. Sex
Sex was not found to be an important predictive factor in
our study (P=.518). This is similar to findings by Gurlek
et al. (1998). In contrast, Hamalainen et al. (1999), Tseng
(2006),Resnick et al. (2004), andHennis et al. (2004)found
sex to be a significant prognostic factorthe male gender
having an increased predisposition to amputation.
3.1.3. Race
Race was not found to be a significant predictive factor
for limb loss in our study. In a study conducted byYoung
et al. (2003), Native Americans, African Americans, and
Hispanics were found to have an increased risk of
amputations compared to the whites.
3.1.4. Type of DFP
Gangrene (Pb.001) and infection (P=.001) were found
to be predictive factors for limb loss in our study. However,osteomyelitis was found to be a significant prognostic factor
byFejfarova et al. (2002)and Gurlek et al. (1998).
3.1.5. Risk factors
Smoking, alcoholism, obesity and hyperlipidaemia were
not found to be predictive factors for limb loss in our study
conducted (PN.05). Smoking was also not found to be a
significant predictive factor byGurlek et al. (1998), Lehto
et al. (1996)andSelby & Zhang (1995).
3.1.6. Comorbidities
Both stroke (P=.028) and IHD (P=.008) were found tobe predictive factors of limb loss in our cohort while
hypertension was not (P=.493). Similarly, stroke was found
to be a significant factor bySelby & Zhang (1995), while
hypertension was not found to be a significant factor by
Gurlek et al. (1998). However, hypertension was found to
be a significant factor by Selby and Zhang.
3.1.7. Complications
PVD (Pb.001) and nephropathy (Pb.001) were found to
be significant predictive factors for limb loss in our cohort.
Studies conducted byHamalainen et al. (1999),Young et al.
(2003), Nelson et al. (1988), Resnick et al. (2004), Lehto
Table 1 (continued)
Risk factor
Limb loss Unadjusted Stepwise analysis
Positive Negative OR (95% CI) Pvalue OR (95% CI) Pvalue
Duration of diabetes
2130 years 11 (37.9) 18 (62.1) 2.4 (0.413.7) .309
GHb level N7% Yes 34 (23.1) 113 (76.9) 0.5 (0.30.9) .034
No 21 (38.2) 34 (61.8) 1.0
Pathogens
MRSA 7 (70.0) 3 (30.0) 7.0 (1.728.1) .006
B. fragilis 7 (35.0) 13 (65.0) 1.5 (0.64.0) .413
Staphylococcus aureus 7 (15.2) 39 (84.8) 0.4 (0.21.0) .042
P. aeruginosa 10 (31.3) 22 (68.8) 1.3 (0.62.9) .578
Streptococcus agalactiae Group B 3 (15.8) 16 (84.2) 0.5 (0.11.7) .249
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et al. (1996), and Selby & Zhang (1995) also found
nephropathy to be a significant prognostic factor. However,
Sheahan et al. (2005)andGurlek et al. (1998) did not find
nephropathy to be a significant predictive factor. Studies
conducted byFejfarova et al. (2002), Gurlek et al, Hennis
et al. (2004), and Lehto et al. also found PVD to be a
significant predictive factor. In contrast, retinopathy was notfound to be a significant factor (PN.05) in our study, similar
to findings by Gurlek et al.
3.1.8. Duration of diabetes
Duration of diabetes was not found to be a predictive
factor for limb loss in our study, similar to findings by
Gurlek et al. (1998). However, duration of diabetes was
found to be a significant factor by Resnick et al. (2004),
Lehto et al. (1996), andSelby & Zhang (1995).
3.1.9. Sensory neuropathy
Presence of sensory neuropathy, as measured by 5.07SemmesWeinstein monofilament test, was found to be a
predictive factor in our study (P=.029), similar to findings
by Gurlek et al. (1998). However, the findings of
Hamalainen et al. (1999), Nelson et al. (1988), Hennis
et al. (2004),Lehto et al. (1996), andSelby & Zhang (1995)
found neuropathy to be a significant factor for limb loss.
3.1.10. ABI measurements
With regard to ABI measurements, patients with ABI
b0.8 (indicating ischaemia) was found to be a highly
significant factor for limb loss (P=.001). The same result
was also achieved by Hamalainen et al. (1999).
3.1.11. Endocrine control
GHb level was found to be a significant predictive factor
for limb loss in this cohort (P=.034), which is similar to
findings by Imran et al. (2006), Miyajima et al. (2006),
Hennis et al. (2004), Resnick et al. (2004), Lehto et al.
(1996), andSelby & Zhang (1995).
3.1.12. Pathogens
When individual pathogens were assessed as predictive
factors for limb loss, MRSA (P=.006) and Staphylococcus
aureus (P=.042) were found to be predictive factors for
limb loss in our study. Fejfarova et al. (2002) foundStaphylococcus aureus to be a significant predictive factor
for limb loss.
4. Conclusions
This is the first prospective study in detail to evaluate the
predictive factors for limb salvage in patients with DFP in
Singapore. Significant univariate predictive factors for limb
loss were age above 60 years, comorbidities (stroke and
IHD), complications of diabetes (nephropathy), PVD,
sensory neuropathy, GHb level, ABI b0.8, DFP such as
gangrene and infection, and pathogens such as MRSA and
Staphylococcus aureus. Upon stepwise logistic regression,
only PVD and infection were significant.
Acknowledgment
The authors would like to thank all members of the NUH
Multi-Disciplinary Team for DFP, Dr. Vikram David, Dr
V.A. Rajesh, Dr Ajay Nambiar, and the house officers and
medical officers of NUH wards for their commitment in
providing health care to patients with DFP.
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3rd International Congress on Pediatrics
and the Metabolic Syndrome
3rd International Congress on Prediabetes and the Metabolic Syndrome Epidemiology,
Management and Prevention of Diabetes and Cardiovascular Disease
Venue: Nice, France
Date: April 14, 2009
For further information, please contact:
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3rd International Congress on Prediabetes and the Metabolic Syndrome
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