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DVD13110.1177/1474651412475098The British Journal of Diabetes and Vascular DiseaseMoosa et al.

Achieving Best Practice

Peripheral arterial disease in diabetic Jordanian


patients and the agreement between ankle
brachial index and toe brachial index

The British Journal of


Diabetes & Vascular Disease
13(1) 3742
The Author(s) 2013
Reprints and permission:
sagepub.co.uk/journalsPermissions.nav
DOI: 10.1177/1474651412475098
dvd.sagepub.com

Sameh R Moosa,1 Faris G Bakri,2 Muhammad R Khammash,3


Hashem Y Jaddou,4 Nawwaf J Shatnawi3 and Kamel M Ajlouni1

Abstract
This study aims to screen patients with type 2 diabetes mellitus for peripheral arterial disease (PAD) and to determine
the agreement between ankle brachial index (ABI) and toe brachial index (TBI). A total of 182 diabetic patients at 40
years of age or older were assessed using both ABI and TBI. Mean age was 60.5 (SD 8.1) years. PAD was present in
28.9% and 5.4% of patients according to TBI and ABI definitions respectively. The prevalence of high ABI (ABI > 1.3) was
16.5%. The agreement between TBI and ABI results was fair. Current smoking was associated with low ABI whereas age
was inversely associated with TBI.We strongly suggest using both the ABI and TBI as screening tests for PAD because the
agreement between these tests was fair, they complement each other in most instances and they detect PAD at different
anatomical levels.
Keywords
ankle brachial index; diabetes mellitus; peripheral arterial disease; peripheral vascular disease; toe brachial index

Introduction
PAD is major complication of T2DM.1 More than 60% of
non-traumatic lower limb amputations occur in diabetic
patients with the main risk factors being peripheral neuropathy and PAD.2
The prevalence of PAD in diabetic patients is variable
and ranges between 8 and 38%.3 In Jordan, however,
there is scarce data on PAD among diabetic patients
despite the high prevalence of T2DM (17%) among the
adult population.4 One study in Jordan looking at
ischemia as defined by ABI < 0.9, found a prevalence of
58% among a sample of 60 inpatients with diabetic foot
infections, 23% of whom had severe ischemia together
with severe infection necessitating major limb amputation.5 Another study performed on hospitalised
Jordanian diabetic patients showed that out of 100
patients, 34 patients had ABI < 0.9.6 Data from our general region are also scarce; in Bahrain, 12% of 1,477 diabetic patients had PAD when assessed by lower limb
pulse palpation.7 Another large multicentre study from
five Middle Eastern countries (United Arab Emirates,
Kuwait, Qatar, Bahrain, and Oman) looking into the
prevalence of PAD among high risk groups showed that
47% of diabetic patients older than 55 years with high
risk for atherosclerosis had ABI 0.9.8

Abbreviations:
ABI ankle brachial index
BMI body mass index
PAD peripheral arterial disease
T2DM type 2 diabetes mellitus
TBI toe brachial index

Screening tests for PAD include clinical assessment


and ABI or TBI. ABI 0.9 and a TBI < 0.7 have been
widely used as cutoff points to define PAD.9 However,
the ABI can be falsely elevated (ABI >1.3) due to medial
arterial calcification that might complicate the diagnosis
1The

National Center for Diabetes Endocrinology and Genetics,


Amman, Jordan
2Jordan University Hospital, Amman, Jordan
3King Abdullah University Hospital, Irbid, Jordan
4Jordan University of Science and Technology, Irbid, Jordan
Corresponding author:
Sameh Rasmi Moosa, The National Center for Diabetes Endocrinology
and Genetics, Queen Rania Street, Building Number: 212, Amman,
13165, Jordan.
Email: sameh.moosa@ncd.org.jo

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38

The British Journal of Diabetes and Vascular Disease 13(1)

of PAD.10 Toe pressure in these situations is believed to


provide an accurate measurement of distal limb systolic
pressure in vessels that do not typically become noncompressible.9 Comparative studies between ABI and
TBI in diabetic patients are very scarce and have shown
conflicting results. Brook et al.11 found that toe pressure
measurement is superior only in patients with overt calcification (ABI 1.3) while Sahli et al.12 proposed that
non-invasive screening measurements for lower limb
ischemia should be combined with both ankle blood
pressure and toe blood pressure.
Atherosclerosis in patients with diabetes occurs predominantly in the below-knee arteries, whereas proximal arteries are relatively free of disease.13 Therefore,
relying only on ABI in the assessment of PAD might
underestimate the prevalence of PAD. TBI, in these situations, can prove to be a useful addition in the diagnosis
of PAD as it measures the arterial pressure in the below
ankle region.
The aim of this study is to determine both the prevalence of PAD and the level of agreement between ABI
and TBI measurements in diabetic patients attending a
tertiary center in Jordan.

Methods
This is a cross-sectional study on patients with T2DM
attending the National Center for Diabetes, Endo
crinology, and Genetics (NCDEG) (Amman, Jordan).
NCDEG is a specialised center providing comprehensive care to diabetic patients from all over the country.
Included patients were 40 years of age or older, had two
or more visits to the center and attended the outpatient
general diabetic clinic every 13 months as part of their
routine follow-up. Exclusion criteria included pregnancy, big toe amputation and known PAD. Patients
were selected randomly and all participants signed a
consent form. The study was approved by the ethical
committee of the NCDEG. Clinical and demographic
data were collected from patient interviews and the
medical records.

mately 4560. Once a steady cyclic waveform motion


appeared on the monitor display then, the cuff was
deflated and the result was recorded as the systolic blood
pressure. The process was then repeated for the other
arm. The higher reading of the two was then taken as
the brachial artery pressure. The same cuff was placed
around the lower third of the leg. The dorsalis pedis
pulse was palpated or identified by the Doppler and the
systolic pressure was obtained as described for the brachial pressure. The process was repeated for the posterior tibial pulse. The pressure of the artery with the
higher reading was considered as the ankle systolic pressure. The ABI was determined as a ratio of the ankle systolic blood pressure to the brachial systolic blood
pressure.
To measure toe pressure, an optimal cuff width of 2.5
cm was placed around the proximal phalanx of the big
toe and the photoplethysmography probe (model PG-21)
was affixed to the pad of the big toe using double-sided
clear tape.15 Once a steady cyclic waveform motion
appeared on the monitor display then the cuff was
deflated and the result was recorded as systolic toe pressure. The test was then repeated on the other foot. The
TBI was calculated as a ratio of the toe systolic blood
pressure to the brachial systolic blood pressure.9 The ABI
and TBI measurements for all patients were performed
by the same investigator (S.R.M.).
A low ABI value of 0.9 was considered to suggest the
presence of PAD, between > 0.9 and 1.3 as normal, and
> 1.3 as high ABI and to suggest medial arterial wall calcification. This cutoff point of > 1.3 was used instead of
other values such as 1.2 or 1.4 because it is used in the
international guidelines and allows comparison with
previous studies.11,16,17 A TBI of 0.7 was considered
normal, while a value of < 0.7 was considered low and
was suggestive of PAD.9 Patients with low or high ABI
readings in one leg were classified in the low or high ABI
groups respectively even if the other leg had normal
reading. The same approach was used for patients with
low TBI.

Statistical analysis

Criteria for PAD evaluation


Brachial systolic pressure, ankle systolic pressure, and
toe systolic pressure were measured by a vascular testing
system (SD30EX, Hadeco, inc., Kawasaki, Japan).
Measurements of ABI and TBI were performed according to the testing system instructions and as reported by
Hiatt et al.14 Briefly, the patients were asked to rest
supine for 1015 minutes, in a room maintained at a
temperature of 2325C. A suitable blood pressure cuff
was wrapped around the upper arm and the brachial
pulse was then palpated and the hand-held Doppler
probe (BT8M, 8 MHz) placed at an angle of approxi-

Statistical analysis was performed using the Statistical


Package for Social Sciences (SPSS, version 17)
and the Cohen kappa statistics package. Chi square
was used to compare the proportions of patients
according to ABI categories with regard to other
variables.
Cohens kappa statistic was used, after excluding
patients with ABI 1.3, to assess the agreement
between ABI and TBI. Landis and Koch classification
for the interpretation of kappa was used (0.20.4 represented fair agreement, 0.40.6 represented moderate
agreement).18 Multiple logistic regression models were

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39

Moosa et al.
Table 1. Demographic and clinical characteristics of study
population (n=182)
Characteristics

n (%)

Age (years)

Gender

Smoking

BMI

T2DM duration (years)

Treatment

HbA1C %

Hypertension

Dyslipidemia

4059
6069
70
Male
Female
Current
Past
Never
Normal
Overweight
Obese
10
> 10
Oral
Insulin
Oral and insulin
<7
7
Yes
No
Yes
No

81 (44.5)
73 (40.1)
28 (15.4)
95 (52.2)
87 (47.8)
31 (17.0)
57 (31.3)
94 (51.7)
16 (8.9)
64 (35.6)
100 (55.6)
99 (54.4)
83 (45.6)
98 (53.8)
14 (7.7)
70 (38.5)
62 (35.8)
111 (64.2)
154 (84.6)
28 (15.4)
159 (87.4)
23 (12.6)

Key: BMI: body mass index; HbA1C: glycated haemoglobin A1C; T2DM:
type 2 diabetes mellitus

used to assess the effect of each of the independent


variables on ABI and TBI after adjusting for potential
confounders. P < 0.05 was considered statistically
significant.

Results
The study population included 182 patients (95 men and
87 women). Ages ranged from 41 to 80 years with a mean
of 60.5 years (SD8.1). The mean duration of diabetes
was 11.5 years (SD7.7). Table 1 shows the population
demographic and clinical characteristics. The study was
performed during the period 1 November 2009 to 30
February 2010.
The prevalence of PAD was 5.4% using the definition
of PAD of ABI < 0.9 and 29% according to TBI < 0.7.
Table 2 shows the population characteristics stratified
according to the ABI results. The prevalence of PAD
increased with age, and was 4.2% in patients < 60 years of
age, 8.1% in patients between 60 and 70 years, and 11% in
patients > 70 years. Of the 10 patients who had low ABI,
nine had low TBI and one had normal TBI (Table 3).
Multiple logistic regression analysis was performed to
test the following independent variables: sex, age, smoking, duration of diabetes and level of glycemic control on
each of ABI and TBI (Table 4). Smoking was the only
variable that was associated with ABI < 0.9. While age
was the only variable that was associated with TBI < 0.7;
with increasing age the risk for TBI < 0.7 increased. The
agreement between ABI and TBI screening was fair
(0.23) according to Cohens kappa statistics.

Discussion
The prevalence of PAD was 5.4% using ABI 0.9 as a definition for PAD. Previous studies using this method showed
variable results ranging between 8.7% and 23.5%.3 Thus,

Table 2. Ankle brachial index (ABI) results stratified according to clinical and sociodemographic characteristics (n=182)
Variable
Sex

DM duration

Smoking

T2DM treatment

Hypertension

BMI

HbA1C%

Male
Female
10 years
>10 years
Current
Past
Never
Oral
Insulin
Oral and Insulin
Yes
No
Normal
Overweight
Obese
<7
7

ABI 0.9 (n=10)

0.9 < ABI 1.3 (n=142)

ABI > 1.3 (n=30)

P value

5 (50%)
5 (50%)
2 (20%)
8 (80%)
3 (30%)
4 (40%)
3 (30%)
3 (30%)
0 (0%)
7 (70%)
9 (90%)
1 (10%)
2 (20%)
1 (10%)
7 (70%)
2 (22.2%)
7 (77.8%)

68 (47.9%)
74 (52.1%)
78 (54.9%)
64 (45.1%)
26 (18.3%)
41 (28.9)
75 (52.8%)
77 (54.2%)
12 (8.5%)
53 (37.3%)
120 (84.5%)
22 (15.5%)
13 (9.3%)
52 (37.1%)
75 (53.6%)
49 (36.6%)
85 (63.4%)

22 (73.3%)
8 (26.7%)
19 (63.3%)
11 (36.7%)
2 (6.7%)
12 (40%)
16 (53.3%)
18 (60%)
2 (6.7%)
10 (33.3%)
25 (83.3%)
5 (16.7%)
1 (3.3%)
11 (36.7%)
18 (60%)
11 (36.7%)
19 (63.3%)

0.040

0.056

0.266

0.285

0.877

0.289

0.682

Key: BMI: body mass index; HbA1C: glycated haemoglobin A1C; T2DM: type 2 diabetes mellitus

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The British Journal of Diabetes and Vascular Disease 13(1)

Table 3.Toe brachial index (TBI) results stratified according to


ankle brachial index (ABI) (n=182)
ABI

TBI of 0.7 n

TBI < 0.7 n

ABI 0.9 (n=10)


0.9 < ABI 1. 3 (n=142)
ABI > 1.3 (n=30)

1
107
25

9
35
5

our results are slightly lower than the reported range. This
could be due to the relatively small percentage (15.4%) of
patients aged more than 70 years in our study (Table 1).
Risk factors associated with low ABI included only
current smoking (Table 4). On the other hand, the prevalence of PAD was 28.9% using TBI < 0.7 as a definition
for PAD and the associated risk factors included only
increasing age.
Our finding that the prevalence of PAD varied between
the two methods of ABI and TBI might be because the
ABI and the TBI detect PAD at different anatomical levels; a low ABI suggests the presence of arterial stenotic
lesions between the aorta and the ankle joint while a low
TBI suggests the presence of stenotic lesions between the
aorta and the toes.19,20 These variations in the prevalence
and in the associated risk factors suggest a difference in
the underlying pathology for the development of PAD in
our study population. Likewise, Aboyanes et al.20 in a prospective study using ABI and TBI to investigate the risk
factors associated with the progression of PAD concluded
that different pathophysiology for the progression of PAD
in large and small vessel is present since the associated
risk factors were different. Sahli et al.12 also suggested that
the differences between ankle and toe blood pressure
measurement could potentially be due to differences in
the pathology between small versus larger arteries.
In our study, the prevalence of high ABI in diabetic
patients is 16.5% which is slightly higher than earlier
reports by both Brooks et al.11 and Suominen et al.16 who

reported prevalences of 9.2% and 12.2% respectively.


Detection of this group of patients is of paramount
importance since high ABI has been associated with
increased all-cause and cardiovascular mortality similar
to low ABI and therefore it is suggested that a high-risk
patient with an elevated ABI should be treated as equivalent to a PAD patient in terms of risk for mortality.10,21,22
The agreement between ABI and TBI measurements
here was fair according to Cohens kappa statistic. This
might be due to the considerable number of patients with
low TBI but normal ABI (Table 3). A previous study by
Brooks et al.11 comparing the ABI and TBI between diabetic patients and non diabetic controls concluded that as
long as ABI is not obviously falsely elevated (i.e. > 1.3), it
gives as much information as TBI and can be relied upon
to make clinical decisions. This is in contrast to our results
that interestingly showed that a considerable percentage
(25%) of our patients had low TBI along with a normal
ABI (Table 3). It should be noted, however, that Brooks et
al.11 used the following different ABI and TBI cut off
points for PAD definition: low ABI of < 0.9, low TBI <
0.54, normal ABI > 0.9 to < 1.3, normal TBI > 0.540.93,
high ABI > 1.3, and high TBI > 0.94. They also did not
separately analyse subjects with impaired peripheral circulation.
Limitations of this study include the lack of comparison to other more sensitive tests such as digital
subtraction, computed tomography or magnetic resonance angiography procedures.9 Therefore, it is highly
possible that the use of ABI could have underestimated the true prevalence of PAD especially as the
sensitivity of ABI is variable and ranges between 15
and 79% and is particularly low in the elderly and in
patients with diabetes.23 Another limitation is the
small number of patients older than 70 years of age
which probably has resulted in a relatively low prevalence of PAD and limited the power to make inferences about other association.

Table 4. Multiple logistic regression analysis on ankle brachial index (ABI) and toe brachial index (TBI) (n=152)
Variable

ABI

Odds ratio (95%)

P value

Odds ratio (95%)

P value

2.194 (0.38212.594)
1
2.222 (0.39412.523)
2.132 (0.27216.732)
5.272 (0.73237.956)
1
4.479 (0.57634.828)
12.845 (1.180139.794)
1.905 (0.31311.607)

0.378
0.632
0.366
0.472
0.099
0.111
0.152
0.036
0.484

1.412 (0.5743.472)
1
2.979 (1.2117.327)
7.138 (2.04424.928)
1.168 (0.4992.732)
1
0.799 (0.2832.257)
1.331 (0.4164.253)
2.244 (0.8825.710)

0.452
0.004
0.017
0.002
0.720
0.718
0.673
0.630
0.090

Sex
Age

T2DM duration
Smoking

HbBA1C%

4060
6069
70
Never
Past
Current

TBI

Key: HbA1C: glycated haemoglobin A1C; T2DM: type 2 diabetes mellitus

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41

Moosa et al.

Key messages

Prevalence of occlusion in the foot is probably more


common than that above the ankle in Jordanian
diabetic patients.
Smoking and age are risk factors for PAD in Jordanian
diabetic patients.
Since agreement between ABI and TBI is fair, screening
for PAD in diabetic patients should include the use of
both ABI and TBI.
Arterial calcification that is indicated by elevated ABI
is common in diabetic patients and needs further
attention from the health care providers.

In conclusion, the prevalence of PAD according to the


use of ABI in diabetic Jordanian patients is generally
slightly lower than the reported rates from other regions.
This, however, should not lead to underestimation of this
problem since the reflected number of affected patients
would be large as the prevalence of diabetes is high in
Jordan. In addition, we highly recommend using both,
the ABI and TBI as screening tests since both complement each other and detect PAD at different levels.
Funding
This research received no specific grant from any funding
agency in the public, commercial, or not for-profit sectors.

Conflict of Interest Statement


The authors declare that they have no conflicts of interest.

Reference
1. Gregg EW, Sorlie P, Paulose-Ram R et al. Prevalence of
lower-extremity disease in the US adult population 40
years of age with and without diabetes: 19992000 national
health and nutrition examination survey. Diabetes Care
2004; 27: 1591-7.
2. Driver VR, Fabbi M, Lavery LA, Gibbons G. The costs of
diabetic foot: the economic case for the limb salvage team.
J Am Podiatr Med Assoc 2010 100: 335-41.
3. Jude EB, Eleftheriadou I, Tentolouris N. Peripheral arterial
disease in diabetes: a review. Diabet Med 2010; 27: 4-14.
4. Ajlouni K, Khader YS, Batieha A et al. An increase in
prevalence of diabetes mellitus in Jordan over 10 years. J
Diabetes Complications 2008; 22: 317-24.
5. Khammash MR, Obeidat KA. Prevalence of ischemia in
diabetic foot infection. World J Surg 2003; 27: 797-9.

6. Khammash MR, Obeidat KA, El-Qarqas EA. Screening of


hospitalised diabetic patients for lower limb ischaemia: is
it necessary? Singapore Med J 2008; 49: 110-13.
7. Al-Mahroos F, Al-Roomi K. Diabetic neuropathy, foot
ulceration, peripheral vascular disease and potential risk
factors among patients with diabetes in Bahrain: a nationwide primary care diabetes clinic-based study. Ann Saudi
Med 2007; 27: 25-31.
8. El-Menyar A, Amin H, Rashdan I et al. Ankle-brachial
index and extent of atherosclerosis in patients from the
Middle East (the AGATHA-ME study): a cross-sectional
multicenter study. Angiology 2009; 60: 329-34.
9. Norgren L, Hiatt WR, Dormandy JA et al. Inter-Society
Consensus for the Management of Peripheral Arterial
Disease (TASC II). J Vasc Surg 2007; 45(suppl S): S5-67.
10. Suominen V, Uurto I, Saarinen J et al. PAD as a risk factor
for mortality among patients with elevated ABI--a clinical
study. Eur J Vasc Endovasc Surg 2010; 39: 316-22.
11. Brooks B, Dean R, Patel S et al. TBI or not TBI: that is the
question. Is it better to measure toe pressure than ankle
pressure in diabetic patients? Diabet Med 2001; 18: 528-32.
12. Sahli D, Eliasson B, Svensson M et al. Assessment of toe
blood pressure is an effective screening method to identify diabetes patients with lower extremity arterial disease.
Angiology 2004; 55: 641-51.
13. Aerden D, Massaad D, von Kemp K et al. The anklebrachial index and the diabetic foot: a troublesome marriage.
Ann Vasc Surg 2011; 25: 770-7.
14. Hiatt WR, Hoag S, Hamman RF. Effect of diagnostic criteria on the prevalence of peripheral arterial disease. The San
Luis Valley Diabetes Study. Circulation 1995; 91: 1472-9.
15. Pahlsson HI, Laskar C, Stark K et al. The optimal cuff width
for measuring toe blood pressure. Angiology 2007; 58: 472-6.
16. Suominen V, Rantanen T, Venermo M et al. Prevalence
and risk factors of PAD among patients with elevated ABI.
Eur J Vasc Endovasc Surg 2008; 35: 709-14.
17. Hirsch AT, Haskal ZJ, Hertzer NR et al. ACC/AHA 2005
Practice Guidelines for the management of patients with
peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic). A collaborative report from
the American Association for Vascular Surgery/Society for
Vascular Surgery, Society for Cardiovascular Angiography
and Interventions, Society for Vascular Medicine and
Biology, Society of Interventional Radiology, and the
ACC/AHA Task Force on Practice Guidelines (Writing
Committee to Develop Guidelines for the Management of
Patients With Peripheral Arterial Disease). Endorsed by the
American Association of Cardiovascular and Pulmonary
Rehabilitation; National Heart, Lung, and Blood Institute;
Society for Vascular Nursing; TransAtlantic Inter-Society
Consensus; and Vascular Disease Foundation. Circulation
2006; 113: e463-654.
18. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977; 33: 159-74.

Downloaded from dvd.sagepub.com by guest on February 16, 2015

42

The British Journal of Diabetes and Vascular Disease 13(1)

19. Morimoto S, Nakajima F, Yurugi T et al. Risk factors


of normal ankle-brachial index and low toe-brachial
index in hemodialysis patients. Ther Apher Dial 2009;
13: 103-07.
20. Aboyans V, Criqui MH, Denenberg JO et al. Risk factors
for progression of peripheral arterial disease in large and
small vessels. Circulation 2006; 113: 2623-9.

21. Resnick HE, Lindsay RS, McDermott MM et al.
Relationship of high and low ankle brachial index to all-

cause and cardiovascular disease mortality: the Strong


Heart Study. Circulation 2004; 109: 733-9.
22. Aboyans V, Ho E, Denenberg JO, Ho LA et al. The association between elevated ankle systolic pressures and peripheral occlusive arterial disease in diabetic and nondiabetic
subjects. J Vasc Surg 2008; 48: 1197-203.
23. Dachun X, Jue L, Liling Z et al. Sensitivity and specificity
of the ankle--brachial index to diagnose peripheral artery
disease: a structured review. Vasc Med 2010; 15: 361-9.

Downloaded from dvd.sagepub.com by guest on February 16, 2015

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