Received:
Revised:
Accepted:
August 7, 2013 October 10, 2013 October 31, 2013
Corresponding Author: Se-Jung Yoon, National Health Insurance Service Ilsan Hospital, 1232 Baeksuk-dong, Ilsandongku, Goyang, Kyunggi-do 410-719, Korea
Tel: +82-31-900-0950, Fax: +82-31-900-0957, E-mail: [email protected]
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pISSN 2287-2892 • eISSN 2288-2561
JLA
The Correlation Between Achilles Tendon Thickness and Cardiovascular Risk Factors
Min-seob Kwak1, Se-Jung Yoon1, Yun-Hyeong Cho2, Suk-Min Hong1, Jong-Kwan Park1, Seungjin Oh1, Dong Woon Jeon1, Joo Young Yang1
1Division of Cardiology, NHIS Ilsan Hospital, 2Division of Cardiology, Myongji Hospital, Goyang, Korea
Background: Achilles tendon thickness (ATT) has been associated with increased cardiovascular risk in patients with familial hypercholesterolemia (FH). The aim of this study is to establish the correlation among ATT, obesity and established cardiovascular risk factors such as diabetes mellitus, hypertension, coronary artery disease, peripheral artery disease, smoking, and dyslipidemia.
Methods: In total, 19 patients (male 31.5%, mean age 60.0±12.5) with dyslipidemia and 96 control (male 64.6%, mean age 62.3±8.5) were enrolled. ATT was measured by ultrasonography. Anterioposterior diameter which represents the ATT was measured bilaterally, 4 cm above the insertion of Achilles tendon to the tuber calcite. Dyslipidemia was defined as elevated total cholesterol, triglyceride, or LDL cholesterol, or low levels of HDL cholesterol.
Results: There was no significant differences including ATT between the two groups (for ATT, dyslipidemia group, 0.44±0.04 vs control, 0.45±0.02 cm, p=0.783). There was no significant correlation between ATT and other cardiovascular risk factors except weight (r=0.34, p=0.007) and body mass index (r=0.63, p<0.001). Dyslipidemia was not significantly correlated with ATT (r=0.02, p=0.783). Use of statin was not significantly correlated with ATT (r=0.04, p=0.605).
Conclusion: ATT was not significantly increased in patients with dyslipidemia. Lipid accumulation of Achilles tendon was not found in patients with dyslipidemia in this study.
Key Words: Dyslipidemia, Achilles tendon, Atherosclerosis
INTRODUCTION
The reduction of risk factors for cardiovascular disease can prevent the incidence of the cardiovascular diseases.
So, the evaluation of an individual’s risk of experiencing a future cardiovascular event increasingly forms the basis of clinical guidelines for the prevention of cardiovascular diseases worldwide.1
Life style risk factors including obesity are strongly associated with established cardiovascular risk factors.2-4
The harmful impact of obesity on the incidence of subsequent cardiovascular disease is partly mediated by increased levels of cardiovascular risk factors, in particular hypertension, dyslipidemia and diabetes.5
Tendon pathology inclusive of Achilles tendon thickness (ATT) has been shown to be associated with fat distri- bution in some previous investigations.6-8 And ATT has been associated with increased cardiovascular risk in patients with familial hypercholesterolemia (FH).9-11
Imaging techniques that have been used for the eva-
luation of ATT are ultrasonography (US), computed tomo- graphy (CT)12,13 and magnetic resonance imaging (MRI).14 Among them, the advantages of ultrasonography are that it is noninvasive, relatively inexpensive, and does not irradiate; hence this measure can be repeatedly performed with no adverse effects on the participant.
We report that assessment of the correlation between ATT and cardiovascular risk factors, especially dyslipidemia, not FH.
MATERIALS AND METHODS 1. Study population
During 2009 and 2010, patients who visited cardio- vascular center of National Health Insurance Service (NHIS) Ilsan hospital for chest pain, hypertension, dyslipidemia, coronary artery occlusive disease (CAOD) or peripheral artery occlusive disease (PAOD) were enrolled. A total of 19 patients (male 31.5%, mean age 60.0±12.5) with dyslipidemia and 96 control (male 64.6%, mean age 62.3±8.5) were enrolled and patients treated with statin were also included. Dyslipidemia was defined if there was at least one of these: high total cholesterol (>240 mg/dL), triglyceride (TG) (>200 mg/dL), LDL-cholesterol (LDL-C,
>160 mg/dL) or low HDL-cholesterol (HDL-C, <40 mg/dL) for low risk group. And the criteria for LDL-C is adapted for very high, high, moderate groups.15
Demographic variables, laboratory data and medication histories were collected. Patients who were diagnosed with or suspected to have familiar hypercholesterolemia were excluded.
This research protocol was complied with ethical prin- ciples for medical research involving human subjects from the World Medical Association Declaration of Helsinki.
And the Institutional Review Board of the National Health Insurance Corporation Ilsan Hospital approved this study.
2. Ultrasonographic measurement of Achilles tendon thickness
The ultrasonographic examination was performed with a real time B-mode scanner with a 5–10MHz electronic linear array transducer (iE33 imaging system, Philips, Andover, MA, US). The optimal focal zone of the trans- ducer was placed at the level of the tendon to assess the tendon structure optimally. Special care was taken to ensure that the probe was parallel to the tendon to avoid the potential artifact of focal hypoechoic areas due to anisotropy. Each ATT was examined ultrasonogra- phically according to a standardized protocol in transverse and longitudinal scans.16,17 Patients were examined in a prone position with both feet hanging free over the edge of the scanning table; the US was performed statically and dynamically. Pressure on the imaged tissue was avoided as much as possible. ATT was measured as the short diameter at the level where the tendon was most thickened. The echo structure of the ATT was considered normal when the typical hypoechoic collagen (fiber bundles) with its hyperechoic internal peritendinea could be seen. US of the patients was performed by one investigator with extensive experience in musculoskeletal ultrasound.
3. Statistical analysis
The SPSS software was used for statistical analyses (release 18.0 for Windows; SPSS, Inc., Chicago, IL, USA).
Between group comparisons were performed using the independent t-test or the Mann–Whitney U test for continuous variables, and the chi-square test or Fisher’s exact test for categorized variables, as appropriate.
Linear correlation analysis was performed between established predictors of cardiovascular disease and ATT in all participants. Pearson correlation coefficients were calculated to assess the validity of the patients, other values compared to the ATT. Statistical hypothesis tests with p
Table 1. Demographic baseline characteristics in two groups
Normal (n=96) Dyslipidemia (n=19) p value
Sex (male, n/%) Age
Height (cm) Weight (kg) BMI (kg/m2) DM (n/%)
Hypertension (n/%) CAOD (n/%) PCI (n/%)
Ischemic stroke (n/%) Smoking
Statin use (n/%) Systolic BP (mmHg) Diastolic BP (mmHg) Heart rate (/min)
62/64.6 62.3±8.5 163.1±8.9 64.4±9.8 24.2±2.6 23/23.9 90/93.8 66/68.7 10/10.4 10/10.4 60/62.5 20/20.8 127.9±16.2 74.7±10.9 74.7±9.9
6/31.5 60.0±12.5 162.5±10.9 66.6±9.0 25.2±1.9 4/21.1 9/47.4 7/36.8 7/36.8 6/31.6 6/31.5 15/78.9 137.5±25.4 66.0±25.6 76.5±12.2
0.525 0.199 0.867 0.557 0.346 0.464 0.191 0.740 0.035 0.028 0.549 0.002 0.141 0.075 0.646 Values are presented as mean±standard deviation or number (%).
BMI; Body mass index, DM; Diabetes mellitus, CAOD; Coronary artery occlusive disease, PCI; Percutaneous coronary intervention, BP; Blood pressure
Table 2. Laboratory data and Achilles tendon thickness in two groups
Normal (n=96) Dyslipidemia (n=19) p value WBC (/µL)
Hb (g/dL) BUN (mg/dL) Creatinine (mg/dL) Fasting sugar (mg/dL) OT (IU/L)
PT (IU/L)
Total Cholesterol (mg/dL) TG (mg/dL)
HDL-C (mg/dL) LDL-C (mg/dL)
Achilles tendon thickness (cm)
6780.4±2422.8 13.7±1.7 14.2±10.1
1.0±1.3 116.5±37.2 29.3±23.1 26.4±14.1 151.5±40.3 117.9±72.1 42.2±10.6 82.0±30.4 0.44±0.04
8400.0±3019.3 14.5±1.4 14.8±9.7 0.8±0.7 122.0±55.1 26.2±10.1 151.5±40.3 155.8±55.6 149.9±87.7 43.1±20.3 77.4±37.2 0.45±0.02
0.097 0.245 0.876 0.652 0.675 0.673 0.882 0.762 0.055 0.832 0.643 0.783 Values are presented as mean±standard deviation or number (%).
BUN; Blood Urea Nitrogen, OT; Glutamic Oxalacetate Transaminase, PT; Glutamic Pyruvate Transaminase, TG; Triglyceride, HDL-C; High density lipoprotein cholesterol, LDL-C; Low density lipoprotein cholesterol
less than 0.05 were considered significant. Values are presented as mean±standard deviation or number (%).
RESULTS
1. Demographic baseline characteristics in two groups
The baseline characteristics of the normal (n=96) and
dyslipidemia (n=19) groups are shown in Table 1. Most demographic characteristics were similar in the two groups (p>0.05), including age, sex, height, weight, BMI, DM, hypertension, CAOD, systolic blood pressure, diastolic blood pressure, heart rate. The proportion of those treated with statin, percutaneous coronary intervention and ischemic stroke showed significantly higher in group of dyslipidemia (p<0.05).
Table 3. Correlation of Achilles tendon thickness and other values
ㅤ Pearson Correlation (r) p value
Age 0.03 0.708
Height 0.17 0.185
Weight 0.34 0.007
BMI 0.63 <0.001
DM 0.01 0.950
Hypertension -0.14 0.132
CAOD 0.08 0.365
PAOD -0.03 0.731
PCI 0.245 0.104
Ischemic stroke 0.412 0.100
Smoking 0.04 0.636
Dyslipidemia 0.02 0.783
Statin use 0.04 0.605
Total Cholesterol -0.09 0.356
TG -0.04 0.629
HDL-C -0.06 0.501
LDL-C -0.03 0.694
BMI; Body mass index, DM; Diabetes mellitus, CAOD; Coronary artery occlusive disease, PAOD; Peripheral artery occlusive disease, PCI; percutaneous coronary intervention, TG;
Triglyceride, HDL-C; High density lipoprotein cholesterol, LDL-C; Low density lipoprotein cholesterol
2. Laboratory data and Achilles tendon thickness in two groups
Laboratory data were similar in the two groups (p>
0.05), including total cholesterol, TG, HDL-C and LDL-C.
There was no significant difference between two groups (for ATT, dyslipidemia group, 0.44±0.04 vs control, 0.45
±0.02 cm, p=0.783). ATT was not significantly increased in patients with dyslipidemia (Table 2).
3. Correlation of Achilles tendon thickness and cardiovascular risk factors
Correlations of ATT and various values were showed in Table 3. Linear correlation analysis revealed a significant correlation between weight, BMI and ATT (for weight, r=0.34, p=0.007; for BMI, r=0.63, p<0.001) (Fig. 1 A and B). ATT was not significantly correlated withage, DM,
hypertension, CAOD, PAOD, percutaneous coronary inter- vention, stroke, dyslipidemia, use of statin. And ATT was not significantly correlated with total cholesterol (r=-0.09, p=0.356), TG (r=-0.04, p=0.629), HDL-C (r=-0.06, p= 0.501) and LDL-C (r=-0.03, p=0.694) (Fig. 1 C-F).
DISCUSSION
Carotid intima-mediathickness (IMT) is very useful and validated marker of atherosclerosis18 and there was a positive correlation between ATT and IMT.19 For the first time higher ATT was found in FH patients with more advanced carotid atherosclerosis, these results may suggest that ATT is associated with carotid atherosclerosis.
Moreover, abnormal Achilles tendon echogenicity may be also associated with carotid atherosclerosis. These results may explain why Achilles tendon xanthomas are associated with premature cardiovascular disease.19 For statin treat- ment, a study presented that statin reduces ATT in FH patients with normal Achilles tendon echostructure.20-23 Atherosclerotic plaque and tendon xanthomas share common mechanisms of lipid accumulation.24 The clue indicating a possible correlation between atherosclerosis and formation of Achilles tendon xanthoma is that patients with both lesions have a similar clinical and biochemical profile.25 Some studies showed lipid profile characteristics of dyslipidemia in subjects who had been with chronic painful midportion Achilles tendinopathy or with Achilles tendon rupture. It showed the possibility of lipid blood levels predisposing individuals to Achilles tendon ruptures.
A higher risk for patients with a pathological lipid status has been described by several authors.25 For metabolic syndrome, there was a study revealed that subjects with chronic painful midportion Achilles tendinopathy have a lipid profile characteristic of a dyslipidemia that is most commonly seen a long side the insulin resistance synd- rome.26,27 So we can suppose that there might be more than simple inflammation of Achilles tendon and also
Fig. 1. Correlation of Achilles tendon thickness and cardiovascular risk factors.
(A and B) Correlation analysis revealed a significance between weight, BMI and Achilles tendon thickness (for weight, r=0.34, p=0.007; for BMI, r=0.63, p<0.001). (C-F) There was no significant correlation between Achilles tendon thickness and other lipid levels.
correlate dyslipidemia or metabolic syndrome with Achilles tendon pathology.
Our study tried to show the difference of ATT between normal and dyslipidemia groups and the correlation between ATT and cardiovascular risk factors (Age, Weight, BMI, DM, Hypertension, CAOD, PAOD, smoking, dyslipi- demia, total cholesterol, TG, HDL-C, LDL-C and statin use).
However, there was no significant difference of ATT between two groups and no significant correlation between ATT and other cardiovascular risk factors except weight and BMI.
The correlation between obesity and ATT has been previously investigated6-8 and Achilles tendon pathology was reported to be correlated with central or peripheral fat distribution.8 Expansion of adipose tissue depots in the upper body and, in particular the abdominal area, is associated with metabolic dysfunction and increased cardiovascular risk.28 As both lipids and insulin resistance play a central role in this relationship, recent findings
associating dyslipidemia and Achilles tendinopathy implicate abdominal fat in the pathoaetiology of Achilles tendinopathy among men.8 Limitations of this study must be acknowledged. First, it was approximately not equal numbers of normal group and dyslipidemia group. The group of dyslipidemia is relatively much smaller than normal group. Second, the sonographic data was perfor- med by a well experienced sonographer but single examiner can cause bias of data and make it difficult to correct the wrong values. And further prospective studies about causality with a larger number of patients are needed.
In conclusion, this study demonstrated that ATT was only significantly positive correlated with BMI and weight however, dyslipidemia was not significantly correlated with ATT. Lipid accumulation of Achilles tendon in dyslipidemia, not FH does not seem to be distinct in this study.
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