|Year : 2020 | Volume
| Issue : 2 | Page : 84-91
B-mode ultrasound assessment of carotid intima–media thickness among adult diabetics and normal adults in Gombe, Northeastern Nigeria
Ibrahim Aishatu Mohammed1, M Yunusa Dahiru2, H Umar Umar3, U Usman Aminu4, T Sa'ad Suleiman4, Philip Oluleke Ibinaiye5, M Dahiru Aminu6, Yusuf Hadiza7
1 Department of Radiology Yobe State University Teaching Hospital, Yola, Nigeria
2 Department of Radiology and Imaging, Federal Medical Centre, Yola, Nigeria
3 Department of Radiology, University of Maiduguri Teaching Hospital, Maiduguri, Nigeria
4 Department of Radiology, Federal Teaching Hospital, Gombe, Nigeria
5 Department of Radiology, Ahmadu Bello University Teaching Hospital, Zaria, Nigeria
6 Department of Histopathology, Federal Medical Centre, Yola, Nigeria
7 Department of Chemical Pathology, Federal Medical Centre, Yola, Nigeria
|Date of Submission||13-Jun-2020|
|Date of Decision||06-Jul-2020|
|Date of Acceptance||21-Jul-2020|
|Date of Web Publication||30-Nov-2020|
M Yunusa Dahiru
Department of Radiology and Imaging, Federal Medical Centre, Yola
Source of Support: None, Conflict of Interest: None
Background: The carotid intima–media thickness (CIMT) has been established as an early predictor of general arteriosclerosis in patients with diabetes. However, there is a paucity of information on CIMT of the common carotid artery (CCA) in healthy patients and in patients with risk factors for cardiovascular diseases such as diabetics, hypertension, and obesity in our environment. The aim of this study was to compare the CIMT in adult patients with diabetes and normal subjects in our institution in Gombe, Northeastern Nigeria. Materials and Methods: This case–control study was conducted over a period of 8 months (from April 2015 to December 2015) at Federal Teaching Hospital, Gombe, on 105 adult diabetic patients and 105 normal adults aged 18 years and above. The CCA was scanned with a PHILIPS HD-9 ultrasound scanner equipped with Doppler facility using a 7.5 MHz linear transducer. Three measurements of the CIMT were obtained at 1 cm proximal to the right and left carotid bulbs and the mean value of the measurements was recorded. Results: The age range of the diabetics comprising 54% of males and 46% of females was 23–79 years, while the range of control group comprising of 53% of males and 47% of females was 18–68 years. The overall mean CIMT (MCIMT) was 0.97 ± 0.4 mm and 0.73 ± 0.1 mm for diabetics and nondiabetic subjects, respectively. MCIMT was significantly higher in diabetics compared to nondiabetic subjects (P = 0.000). In diabetics, overall MCIMT values were 0.96 ± 0.2 mm and 0.91 ± 0.2 mm on the right and left sides, respectively, with a statistically significant difference between the two sides (P = 0.000), while in the normal group, the overall MCIMT values on the right and left sides were 0.75 ± 0.1 mm and 0.73 ± 0.1 mm, respectively, with a statistically significant difference between the two sides (P = 0.021). Furthermore, CIMT correlated positively with age in both diabetic and control groups. Conclusion: This study has shown a statistically significant increase in CIMT in diabetics compared to nondiabetics and age shows a significant correlation with CIMT. Reference value for CIMT in nondiabetic subjects in Northeastern Nigeria has been obtained.
Keywords: Adult diabetics, B-mode ultrasound, carotid intima–media thickness, normal adults
|How to cite this article:|
Mohammed IA, Dahiru M Y, Umar H U, Aminu U U, Suleiman T S, Ibinaiye PO, Aminu M D, Hadiza Y. B-mode ultrasound assessment of carotid intima–media thickness among adult diabetics and normal adults in Gombe, Northeastern Nigeria. J Radiat Med Trop 2020;1:84-91
|How to cite this URL:|
Mohammed IA, Dahiru M Y, Umar H U, Aminu U U, Suleiman T S, Ibinaiye PO, Aminu M D, Hadiza Y. B-mode ultrasound assessment of carotid intima–media thickness among adult diabetics and normal adults in Gombe, Northeastern Nigeria. J Radiat Med Trop [serial online] 2020 [cited 2021 Aug 4];1:84-91. Available from: http://www.jrmt.org/text.asp?2020/1/2/84/301894
| Introduction|| |
Diabetes mellitus (DM) is a chronic medical condition in which the fasting blood sugar (FBS) is elevated greater or equal to 7 mmol/L (126 mg/dl) or 2-h postprandial plasma glucose is greater or equal to 11.1 mmol/L (200 mg/dl). It is an important risk factor for coronary heart disease,, and stroke., DM is a major cause of mortality and morbidity which may lead to permanent disabilities such as blindness, limb amputation, impotence, chronic renal failure, stillbirths, and miscarriages.
DM is classified on the basis of the pathogenic process that leads to hyperglycemia, as opposed to earlier criteria based on the age of onset or the type of therapy. The two broad categories of DM are designated Type 1 and Type 2. Patients with diabetics may present with complications such as chronic leg ulcers, stroke, myocardial infarction, diabetic ketoacidosis, renal failure, recurrent infections, and erectile dysfunction.
About 6% of the world's adults currently have DM occasioned by the adoption of western dietary regimen, lifestyle, and increasing stress from urbanization. The prevalence of DM is expected to triple in Africa and Asia in the nearest feature. The national survey report led by Akinkugbe showed that the prevalence varied from 0.65% in rural Mangu (Plateau State) to 11% in urban Lagos of Nigeria. In the University of Port Harcourt Teaching Hospital, diabetes accounted for approximately 14% of all new cases seen in the medical clinics and over 18% of all the medical outpatient consultations.
Diabetes is a risk factor for the development of atherosclerosis, a systemic condition primarily affecting elastic arteries (carotid arteries and aorta) as it causes arterial wall thickening with subsequent atheroma formation. Studies have consistently demonstrated a positive association between DM and atherosclerotic cardiovascular disease (CVD). Diabetes directly promotes endothelial injury, low-density lipoprotein uptake, or smooth muscle proliferation. For example, insulin has been shown to enhance cholesterol transport into the arteriolar smooth muscle cells and to increase the proliferation and cholesterol synthesis of these cells. Diabetes is one of the risk factors for stroke, myocardial infarction, peripheral vascular disease, and chronic kidney disease.
Assessment of subclinical and clinical target organ damage is a key element in the management of patients with diabetes. Thus, the practical examination for predicting organ damage is the B-mode ultrasonographic measurements of intima–media thickness (IMT) of the carotid arteries. Carotid ultrasonography is able to provide accurate measurements of the thickness of the intima and media of the carotid arteries. Previous studies have shown associations between common carotid artery (CCA) IMT and cardiovascular risk factors,,, the prevalence of CVD,,, and the involvement of other arterial beds with atherosclerosis.,,
High-resolution B-mode ultrasonography is a relatively cheap, safe, noninvasive, reproducible, and precise method of examining and evaluating the walls of CCA for arterial wall thickening and atherosclerotic progression or regression. This modality not only provides a measure of carotid IMT (CIMT) but also detects the presence of plaques and vessel narrowing in patients with diabetes. The thickening of the intima–media complex reflects generalized atherosclerosis, and assessment of CIMT has been proposed as a noninvasive measure of CVD burden in adults. In view of their size, limited movement, and accessibility, the extracranial carotid arteries provide excellent and reproducible sites for IMT assessment.
In this study, the aim is to compare CIMT between diabetic patients and nondiabetic healthy volunteers at Gombe, Northeastern Nigeria.
| Materials and Methods|| |
This hospital-based prospective case–control study was carried out over a period of 8 months from April 2015 to December 2015 at our institution in Gombe, Northeastern Nigeria. Patients were recruited consecutively based on the study inclusion criteria.
The study population consisted of two groups; Group A consisted of patients with diabetes who attended the Endocrinology clinic or were admitted to the medical ward and met the inclusion criteria of the study. Group B (control) comprised apparently normal age- and sex-matched individuals who attended the general outpatient department for a routine medical check.
Inclusion criteria for case group
Subjects of 18 years and above and those who were diagnosed with type 2 DM, based on the WHO criteria, i.e., random blood glucose >200 mg/dl (11.1 mmol/L) and/or fasting plasma glucose (FPG) >126 mg/dl (7 mmol/L) or those on antidiabetic medications for the above indication were considered diabetic in the study (blood glucose values were obtained from the patient's folder).
Exclusion criteria for case group
Pregnant women because of physiological changes and accompanying dilation of CCA, subjects below 18 years, patients with other associated cardiovascular risk factors such as hypertension, smoking, and hypercholesterolemia, and subjects in whom imaging circumstances were very poor, with limited boundary visualization of CCA due to anatomical constraint either a high carotid artery bifurcation or a short neck, were exclusion criteria for case group.
Inclusion criteria for control group
Age-matched healthy males and females aged 18 years and above were inclusion criteria for control group.
Exclusion criteria for control group
Pregnant women, subjects below 18 years, and patients with other associated cardiovascular risk factors such as hypertension, smoking, and hypercholesterolemia were exclusion criteria for control group.
A well-structured data sheet was used to record the patient's biodata and CIMT measurements after informed written consent was obtained from the subjects before enlisting into the study. Approval to carry out the study was obtained from the ethical committee of our institution and also in accordance with the Helsinki Declaration of 1975, as revised in 2000. The subjects were informed on the safety of ultrasound scan and were guaranteed freedom to withdraw from the study at any stage without consequences. The data collected from the participants were recorded serially and kept with the utmost confidentiality.
This study was carried out on 210 subjects made up of 105 diabetic and 105 nondiabetic normal males and females aged 18 years and above who were willing to participate in the study. The nature of examination was explained to each subject and a brief history was obtained. Biodata which included age and sex were recorded for each patient. The controls had their blood samples taken as appropriate for FPG. Those subjects with normal FPG and normal total cholesterol levels were recruited for the study as controls. The height (m) and weight (kg) of each subject were taken using meter ruler and beam weighing scale, respectively. The body mass index (BMI) was calculated as the ratio of the measured weight to the square of the measured height (kg/m2) and categorized using the WHO classification.
The examination of the CCA was performed using a 7.5 MHz linear transducer of a Philips HD 9 ultrasound scanner (Korea 2010). The B-mode grayscale ultrasound scan of the CCA was performed with the subject lying supine with pillow support under the neck to achieve the desired neck extension and head turned 45° away from the side being scanned. An adequate amount of coupling gel was applied to the scan area to eliminate the air gap between probe and skin surface.
The carotid artery was imaged in a longitudinal plane spanning from the superior aspect of the clavicle to the angle of the mandible, with the transducer placed approximately 45° to the skin surface. The carotid bifurcation appears distal to the carotid bulb, while the CCA appears proximal to the carotid bulb, as seen in [Figure 1].
|Figure 1: Grayscale longitudinal image of common carotid artery, carotid bulb (B) and bifurcation into external carotid artery, and internal carotid artery|
Click here to view
Right and left CCAs were examined by multiple longitudinal and transverse scans. The study protocol involved scanning of the far wall of the right and left CCAs at 1 cm proximal to the bulb. This is because IMT values from the near wall depend heavily on gain settings and are therefore less reliable.
The technique of measurement of the CIMT used in this study (1 cm proximal to the carotid bulb) was adopted because the method is simple, reliable, and reproducible. There were minimal inter- and intraobserver errors which were achieved by measuring at the fix mentioned point and three measurements were obtained with average taken, respectively. This method allows for quick identification of the target area and ensures that an identical area is easily assessed on follow-up scans.
Three repeated measurements of CIMT were obtained (mm) in the longitudinal plane at the point of maximal thickness on the far wall of both CCA 1 cm proximal to the carotid bulb where it is clear of plaques. The position of the carotid bulb is defined as the point where the far wall deviated away from the parallel plane of the distal CCA [Figure 1]. The CIMT is the distance between the inner echogenic line representing the intima–blood interface and the outer echogenic line representing the adventitia–media junction with the hypoechoeic media interposed between them [Figure 2]. Measurements were repeated three times on each side, unfreezing on each occasion and relocating the position of maximal IMT. The mean of the three measurements was recorded (mm). The overall mean was arrived at by averaging the mean of the right CIMT (RCIMT) and left CIMT (LCIMT) of diabetic and normal subjects.
|Figure 2: A longitudinal sonogram showing the layers of the carotid artery wall. Arrows A, B, and C representing the intima, media, and adventitia, respectively as two parallel echogenic lines separated by hypoechoic space|
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The data obtained from the subjects were recorded in the datasheet and was analyzed using Statistical Package for the Social Sciences (SPSS) for Windows version 20.0 (SPSS Inc., Chicago, Illinois, USA). Mean ± standard deviation was used to summarize the variables. Comparison of mean and proportion was considered statistically significant if P value was ≤ 0.05. The results were presented in the form of tables, bar charts, and graphs.
| Results|| |
A total of 210 consenting adults comprising 105 diabetic patients and 105 normal adults aged 18 years and above were enrolled in this study. In overall, 113 (53.8%) subjects of which were males and 97 (46.2%) were females. In the diabetic group, 54.3% were male, while 45.7% were female. Conversely, males constituted 53.3% and females 46.7% in the normal.
The age range for the diabetic group was 23–79 years with a mean of 51.81 ± 12.16 years, while in the normal group, the age range was 18–68 years with a mean of 51.19 ± 12.74 years (P = 0.656). The predominant age group in the diabetic group, nondiabetic group, and entire study population is 41–50 years representing 27.6%, 28.6%, and 28.1%, respectively. [Figure 3] shows the distribution of age group in the study population and [Table 1] Shows the mean values of the characteristic features of the study population including the weight, height, BMI, and FBS.
|Figure 3: A bar chart showing the distribution of age and its frequency in the study population|
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The overall mean CIMT (MCIMT) for the diabetic group in this study was 0.97 ± 0.4 mm and 0.73 ± 0.1 mm for the nondiabetic group. There was a statistically significant difference in the CIMT between the two groups (P ≤ 0.001), as shown in [Table 2]. In the diabetic subjects, the overall right and left MCIMT was 0.96 ± 0.2 mm and 0.91 ± 0.2 mm respectively. The difference in CIMT between the right and left sides was statistically significant in both diabetics (P ≤ 0.001) and nondiabetics (P = 0.021). The median CIMT was 0.095 mm and 0.070 mm for the diabetic and nondiabetic groups, respectively.
|Table 2: The difference in mean carotid intima-media thickness between the diabetic and nondiabetic groups|
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The overall MCIMT for male and female diabetics was 1.03 ± 0.6 mm and 0.91 ± 0.2 mm, respectively. The MCIMT values in males were higher than the female values. However, this was not statistically significant in both diabetics (P = 0.145) and nondiabetics (P = 0.071), as shown in [Table 3].
|Table 3: The differences between male and female mean carotid intima-media thickness|
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In the diabetic group, 39.0% had bilaterally thickened CIMT (>0.09 mm) and 10.7% and 4.8% patients had thickened CIMT on the right and left, respectively, while the remaining 45.5% of the patients had normal CIMT. All the nondiabetics had normal CIMT.
In both the diabetic and normal groups, age had a positive correlation with CIMT (P ≤ 0.001), as shown in [Table 4]. [Figure 4] and [Figure 5] also show a significant positive correlation of the CIMT and age. [Table 4] also shows the correlation of weight, height, BMI, and FBS with CIMT in both diabetics and nondiabetics. In both the diabetic and nondiabetic groups, there was a weak negative correlation of the RCIMT and LCIMT with the BMI which was statistically insignificant. While the correlation of the MCIMT with BMI in the diabetic group was weakly positive, an inverse correlation of the MCIMT with BMI was noted in the nondiabetics and both of these correlations were statistically insignificant. After controlling for age, an insignificant effect of BMI on CIMT was observed in both the study groups. There was an insignificant, weak negative correlation of the MCIMT with FBS in the diabetics, as shown in [Table 4]. There was no significant statistical relationship of CIMT with sex except in normal subjects in the RCIMT, as shown in [Table 5].
|Table 4: Correlation of the mean carotid intima-media thickness with age, body mass index, and fasting blood sugar|
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|Figure 4: A graph showing the relationship between right carotid intima–media thickness and age group in diabetics and nondiabetics|
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|Figure 5: The relationship between left carotid intima–media thickness and age group in diabetics and nondiabetics|
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| Discussion|| |
This study revealed that a large proportion of the diabetic population were within the age group 41–50 years, as majority of the diabetic patients attending the endocrinology clinic in our center fall within this age group. Furthermore, a study by Wild et al. on the global prevalence of diabetes has further supported the increasing incidence of diabetes in these age groups due to population growth, urbanization, increasing prevalence of obesity, and physical inactivity in addition to the fact that data on diabetes in the younger age group are limited.
This study showed that CIMT is significantly increased in diabetic patients compared with nondiabetic subjects in both men and women. The MCIMT in the diabetics studied was 0.97 ± 0.4 mm compared to 0.73 ± 0.1 mm in the age- and sex-matched controls and based on the findings in this study, there is increased tendency to atherosclerotic CVD in diabetics going by their CIMT values. Other studies with similar findings include those of Mohan et al. in India where mean IMT values in diabetics were found to be 0.95 ± 0.31 mm which was significantly higher than that of the nondiabetic group which was recorded as 0.74 ± 0.14 mm. Pujia et al. also studied age- and sex-matched diabetics and controls in Italy and found significantly higher CIMT of 0.77 ± 0.13 mm in the diabetics than in the controls in whom the CIMT was 0.69 ± 0.10 mm. Similarly, Geroulakos et al. reported higher CIMT values of 0.82 ± 0.22 mm in diabetics than in controls in whom the CIMT was 0.66 ± 0.13 mm. Although Mohan et al. recorded a higher MCIMT in the diabetics than in the normal, this difference became statistically significant only after the age of 50 years. This difference could be due to racial factor as their study was carried out in a Caucasians or perhaps due to their small sample size. However, Pujia et al. and Geroulakos et al. reported values which are very similar to values recorded in our study despite using the same Caucasian population. This may suggest interplay of other variables such as socioeconomic factors and lifestyle. Bonora et al. in a similar study in Italy reported higher MCIMT in both diabetics and nondiabetics of 1.44 ± 0.15 mm and 1.19 ± 0.15 mm, respectively, compared to our finding. This might be because of the low sample size they used in their study and also could be due racial factors.
Studies conducted in regions with a similar sociocultural background as the index study showed similar findings. Dambatta et al. studied the CIMT in normal adults in Kano, Nigeria, where they found MCIMT to be 0.71 ± 0.10 mm on the right and 0.72 ± 0.10 mm on the left. Yusuf measured the CIMT among diabetic patients in Kano, Nigeria, and documented values of CIMT among diabetics as 0.94 ± 0.29 mm on the right and 1.04 ± 0.38 mm on the left. Ahmadu also studied on diabetics in Maiduguri, Northeastern Nigeria and recorded RCIMT of 0.85 ± 0.18 mm and LCIMT of 0.89 ± 0.16 mm on the right side and left side, respectively. This further buttresses the fact that DM on its own contributes to cardiovascular morbidity and mortality as showed by the above CIMT findings.
This study showed that males had higher values of CIMT than females in the diabetic group. However, it did not attain statistical significance. Similarly, males had higher values of CIMT in the normal which was also statistically insignificant except for the RCIMT, where this gender difference in CIMT was found to be statistically significant (P = 0.014). The higher MCIMT values found in males may be associated with the generally higher prevalence of DM and hypertension among males in our environment. The findings in this study were similar to those of Yusuf. Similarly, De Freitas et al. also noted an insignificant difference in CIMT by gender in their study at São Paulo. Furthermore, Pujia et al. found that, after correcting for age, the higher values of CIMT recorded in the male diabetic patients compared to the females were not statistically significant. On the contrary, Ahmadu reported a statistically significant difference of CIMT in his study with the males having higher values than the females. Furthermore, Zhao et al. who studied on diabetic patients reported a progressive increase in CIMT which was significantly higher in males than females which is in contrast to our observation in this study. This could be because of their larger sample size and a longer period of study and follow-up compared to this study.
In the index study, the RCIMT was found to be significantly higher than the LCIMT in both the diabetic (P ≤ 0.001) and normal subjects (P = 0.021). This finding is contrary to the findings of Yusuf and Ahmadu where the LCIMT values were higher than the RCIMT. On the contrary, Butt and Zakaria study of diabetic patients in Lahore, Pakistan, observed no statistically significant difference between the CIMT on the right and left sides.
In the index study also, the correlation between CIMT and age was noted to be strong when both the sides, i.e., right and LCIMT, were considered independently rather than MCIMT of both sides in the diabetic group. However, in the nondiabetics, all subsets of CIMT measurements showed a strong positive correlation with age. Similarly, Pujia et al. found a positive correlation between CIMT and age in both the diabetic subjects and control group. In addition, Frost et al. also showed a strong positive correlation between CIMT and age in diabetics. Mohan et al. reported that there was a moderate positive correlation between CIMT and age in both diabetics and normal in southern India. On the contrary, Butt and Zakaria reported that there was no correlation between CIMT and age among the three groups of patients younger than 70 years of age but a strong positive correlation which is statistically significant in those above 70 years. Furthermore, Bonora et al. reported no correlation between CIMT and age in diabetics but observed a strong positive correlation of CIMT with age in the nondiabetic group in their study.
In this study, there is a weak positive correlation of the MCIMT with BMI in the diabetics, all of which are statistically insignificant. In the nondiabetic group, a weak inverse correlation of CIMT with BMI which is not significant was noted. However, the analysis of covariance showed that BMI was not independently associated with CIMT in both the diabetic and nondiabetic groups. Studies by Mohan et al. and Pujia et al. also found a weak positive insignificant correlation between MCIMT and BMI in the diabetics consistent which is consistent with the findings in this study. Although Bonora et al. showed that CIMT was not independently associated with BMI in the diabetic group similar to findings in this study, they however found a weak positive correlation between CIMT and BMI in their normals. This may be because they recorded significantly higher mean BMI in their normal subjects compared to the mean BMI in the same group in this study.
Limitations of the study
In view of the financial constraints, the duration of diabetes was not taken into consideration in this study as that will increase financial burdens for the authors. Furthermore, the variability of CIMT with the cardiac circle was not considered, as a capability for gating was not available.
| Conclusion|| |
CIMT obtained by B-mode ultrasonography is higher in subjects with diabetes compared to age- and sex-matched control subjects. This study highlighted a strong positive correlation of CIMT with age in both diabetics and normal. The B-mode measurement of the CIMT is a noninvasive, relatively cheap, and easily accessible procedure to detect early atherosclerosis in diabetics. This may enhance follow-up management of diabetic patients and to investigate the progression/regression of atherosclerosis and monitor the effects of different treatments.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]