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Saudi Journal of Kidney Diseases and Transplantation
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Table of Contents   
RENAL DATA FROM ASIA–AFRICA  
Year : 2018  |  Volume : 29  |  Issue : 3  |  Page : 649-657
Albuminuria status and patterns of dyslipidemia among type 2 diabetes black patients managed at a tertiary health-care hospital: A Post hoc analysis


1 Department of Internal Medicine, Division of Nephrology, University Hospital of Kinshasa, University of Kinshasa, Kinshasa, Democratic Republic of Congo
2 Department of Internal Medicine, Division of Nephrology, University Hospital of Kinshasa, University of Kinshasa, Kinshasa; Faculty of Medicine, University of Kikwit, Kikwit, Democratic Republic of Congo

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Date of Submission31-May-2016
Date of Acceptance26-Jul-2016
Date of Web Publication28-Jun-2018
 

   Abstract 

Cardiovascular disease (CVD) risk in type 2 diabetes mellitus (T2DM) increases with the development of albuminuria and is related in part to dyslipidemia. The present analysis assessed lipid profile and patterns of dyslipidemia in T2DM patients according to albuminuria status. This was a post hoc analysis of data from 181 T2DM patients seen at a tertiary health-care hospital and enrolled in a cross-sectional study of albuminuria status. Abnormal albuminuria was defined as microalbuminuria [albumin to creatinine ratio (ACR) 30-299.9 mg/g] or macro-albuminuria (ACR ≥300 mg/g). Atherogenic dyslipidemia was defined as triglycerides (TGs) ≥150 mg/dL and/or high-density lipoprotein-cholesterol (HDL-c) <40 mg/dL in men and <50 mg/dL in women using international consensus criteria. High levels of total cholesterol (TC), low-density lipoprotein-cholesterol (LDL-c), HDL-c, non-HDL-c, TG, and low level of HDL-c were defined according to 2012 American Association of Clinical Endocrinologists' guidelines. Comparisons between T2DM patients with and without abnormal albuminuria were done using Chi-square test, Student's t-test, or two-sample t-test with equal variance and Mann-Whitney test as appropriate. P< 0.05 defined the level of statistical significance. Of the 181 T2DM patients, 93 (51%) had abnormal albuminuria with 32% and 19% having microalbuminuria and macro-albuminuria, respectively. Average TC, HDL-c, HDL-c, non-HDL-c, and TG levels were 171 ± 41, 111 ± 36, 38 ± 16, 133 ± 38, and 98 (45-234) mg/dL, respectively. These values were significantly lower for TC (P = 0.047), LDL-c (P = 0.030), and non-HDL-c (P = 0.05) in comparison with patients with normal albuminuria. Low HDL-c (64.5%) and high TG (9.7%) were, respectively, the most and less frequent patterns of isolated dyslipidemia in patients with abnormal albuminuria. Atherogenic dyslipidemia with mainly low HDL-c levels is common in T2DM patients with abnormal albuminuria and could contribute to CVD and renal disease progression.

How to cite this article:
Kajingulu FM, Lepira FB, Mbutiwi FI, Makulo JR, Sumaili EK, Bukabau JB, Mokoli VM, Longo AL, Nseka NM. Albuminuria status and patterns of dyslipidemia among type 2 diabetes black patients managed at a tertiary health-care hospital: A Post hoc analysis. Saudi J Kidney Dis Transpl 2018;29:649-57

How to cite this URL:
Kajingulu FM, Lepira FB, Mbutiwi FI, Makulo JR, Sumaili EK, Bukabau JB, Mokoli VM, Longo AL, Nseka NM. Albuminuria status and patterns of dyslipidemia among type 2 diabetes black patients managed at a tertiary health-care hospital: A Post hoc analysis. Saudi J Kidney Dis Transpl [serial online] 2018 [cited 2022 May 23];29:649-57. Available from: https://www.sjkdt.org/text.asp?2018/29/3/649/235175

   Introduction Top


Type 2 diabetic patients are at increased risk for cardiovascular disease (CVD) with myocardial infarction being the leading cause of death in Western studies.[1] Therefore, achieving a better understanding of traditional and emergent CVD risk factors and dietary influences underlying atherogenic dyslipidemia may provide clues to improved interventions to reduce the risk of CVD in high-risk individuals.[1] Among traditional CVD risk factors, dyslipi-demia with mainly increased levels low-density lipoprotein-cholesterol (LDL-c) has been reported to play a central role in the dynamic process of atherosclerosis[2],[3] and explains why current guidelines recommend intensive lowering of LDL-c with statins in an attempt to reduce CV risk.[4] However, concentrations of total cholesterol (TC) and LDL-c in type 2 diabetes are reportedly often similar to levels found in controls,[5] and the common pattern of dyslipidemia of type 2 diabetes, called combined dyslipidemia or atherogenic dyslipidemia, is characterized by low levels of high-density lipoprotein-choles-terol (HDL-c) and elevated triglyceride (TG) levels.[5],[6],[7] This pattern of dyslipidemia that responds better to fibrates has been thought to explain the residual CVD risk observed in statin-treated patients with optimal or near-optimal LDL-c levels.[7],[8],[9] Clinical studies have suggested that abnormal albuminuria (micro-albuminuria and macroalbuminuria) is accompanied by characteristic atherogenic dyslipi-demia,[10],[11],[12] one could expect type 2 diabetes patients with abnormal albuminuria to be at increased risk for CVD.

In Democratic Republic of the Congo, the prevalence of microalbuminuria and macro-albuminuria in patients with diabetes has been reported to be of 45.2% and 12%, respectively.[13] A previous study showed that type 2 diabetes patients with subclinical atherosclerosis had in average low HDL-c and high TG levels compared to those without atheroscle-rosis;[14] however, the frequency of atherogenic dyslipidemia as combined dyslipidemia was not evaluated. The aim of the present post hoc analysis was to evaluate the frequency and patterns of dyslipidemia among type 2 diabetes patients with abnormal albuminuria seen at the University of Kinshasa Hospital.


   Subjects and Methods Top


To determine the patterns of dyslipidemia, we performed a post hoc analysis of data from 181 type 2 diabetes patients enrolled in a cross-sectional study of abnormal albuminuria carried out at the University of Kinshasa Hospital from July 1 to October 30, 2007. The study received the approval of the Ethics Committee of Kinshasa Public School of Medicine and was conducted in accordance with Helsinki Declaration. The details of the study have already been described else-where.[15],[16],[17] In brief, albuminuria as urinary albumin-to-creatinine ratio (ACR) was determined in morning spot urine using immuno-assay method with an automatic device DCA Bayer 2000® (Bayer Health Care LLC, Indiana, USA). Normal albuminuria, micro-albuminuria, and macro-albuminuria were defined as ACR <30, 30–299, and >300 mg/g, respectively.[18] Abnormal albuminuria was defined by the presence of microalbuminuria or macroalbuminuria. Abbreviated modification of diet in renal diseases (MDRD) equation was used to estimate glomerular filtration rate (eGFR).[19] Fasting cholesterol and its sub fractions as well as TG were determined using enzymatic methods with an automatic device Cholestech LDX® (Cholestech Corporation, USA). LDL-c was calculated using the Friedewald formula for patients with TG levels <400 mg/dL.[18],[20] Non-HDL-c, as a surrogate marker of apolipoprotein B (Apo B), was calculated as TC - HDL-c. American Association of Clinical Endocrinologists' Guidelines for Management of Dyslipidemia and Prevention of Atherosclerosis[19],[21] were used to classify isolated patterns of dyslipi-demia as follows: high TC levels as values ≥200 mg/dL, high LDL-c levels as values ≥130 mg/dL, low HDL-c levels as values <40 mg/dL in men and <50 mg/dL in women, high non HDL-c as values ≥160 mg/dL, and high TG levels as values ≥150 mg/dL. Atherogenic dyslipidemia or combined dyslipidemia was defined using both the conventional previous defini-tion (HDL-c <40 mg/dL in men, <50 mg/dL in women, and TG ≥150 mg/dL for both gender) and the 2013 International Consensus.[22] Harmonized definition was used to assess the presence of metabolic syndrome (MetS).[23] Hypertension was defined according to JNC 8 as systolic (SBP) and diastolic (DBP) blood pressures ≥140 and 90 mm Hg, respectively, or history of current antihypertensive drug therapy.[24]


   Results Top


Study population general characteristics

Demographic, clinical, and biological characteristics of the whole group and by albuminuria status are depicted in [Table 1]. One hundred and eighty-one T2DM patients, 53% men, were included in the present post hoc analysis. Their mean age was 56 ±11 years with a median duration of diabetes of 4 (1–32) years; smoking, metabolic syndrome, hypertension, and diabetic retinopathy were present in 8%, 70%, 77%, and 80% of patients, respectively.
Table 1: General characteristics of the whole study population and according to albuminuria status.

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Abnormal albuminuria was present in 93 patients (51%) of whom 32% and 19% had microalbuminuria and macroalbuminuria, respectively [Table 1]. They tended to be older (58 ± 12 vs. 55 ± 10 years) than those with normal albuminuria; however, the difference was not statistically significant (P = 0.075). They also had in average significantly longer diabetes duration [6 (1-32) vs. 3 (1-25); P <0.001], higher SBP (145 ± 28 vs. 136 ± 20 mm Hg; P = 0.006) and PP (57 ± 20 vs. 50 ± 14 mm Hg; P = 0.004), and lower body mass index (BMI) (24.2 ± 4.9 vs. 26.9 ± 4.9 Kg/m2) and waist circumference (87 ± 13 vs. 94 ± 10 cm; P = 0.001) compared to those with normo-albuminuria.

Average levels of fasting blood glucose, glycated hemoglobin, serum creatinine, MDRD-GFR, and ACR for the whole group were 165 (50–445) mg/dL, 9.0 (4.5–14.0), 1.1 (0.433.6) mg/dL, 75 (2–234) mL/min/1.73 m2, and 30 (3–7300) mg/g [Table 1]. Compared to patients with normalalbuminuria, those with abnormal albuminuria had in average significantly higher serum creatinine levels [1.3 (0.5–33.6) vs. 1.1 (0.4–4.1) mg/dL; P <0.001] and lower MDRD-eGFR levels [67 (2–234) vs. 83 (14–211) mL/min/1.73 m2; P<0.001].

Antihypertensive and antidiabetic regimens in the whole group and by albuminuria status are summarized in [Table 2]. The proportion of participants receiving renin-angiotensin system (RAS) inhibitors was significantly (P = 0.010) elevated in patients with abnormal albuminuria than those with normal albuminuria. The differences observed in antidiabetic treatment between the two subgroups did not reach the level of statistical significance [Table 2].
Table 2: Antidiabetic and antihypertensive drug classes in the whole study population and according to albuminuria status.

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Lipid profile in the study population

Lipid and lipoprotein levels of the whole group and by albuminuria status are given in [Table 3]. Average levels of TC, LDL-c, HDLc, non-HDL-c, and TG in the whole group were 177 ± 43 mg/dL, 117 ± 40 mg/dL, 38 ± 15 mg/dL, 139 ± 40 mg/dL, and 100 (45-102) mg/dL, respectively. Patients with abnormal albuminuria had in average significantly lower TC (171 ± 41 vs. 184 ± 43 mg/dL; P = 0.047), LDL-c (111 ± 36 vs. 123 ± 43 mg/dL; P = 0.033), and non-HDL-c (133 ± 38 vs. 146 ± 42 mg/dL; P = 0.025) [Table 3].
Table 3: Lipid profile and patterns of dyslipidemia in the whole study population and according to albuminuria status.

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Patterns of dyslipidemia in the study population

The frequency of isolated and atherogenic dyslipidemia in the whole group and by albuminuria status is reported in [Table 3]. Elevated TC, LDL-c, non-HDL-c, TG, and low HDL-c were found in 30.9%, 39.8%, 32.6%,17.1%, and 67.4% of the whole group patients, respectively. These proportions were 25.8%, 32.3%, 26.9 %, 17.2%, and 64.5% in patients with abnormal albuminuria, respectively. Compared to patients with normal albuminuria, those with abnormal albuminuria had significantly lower proportions of elevated LDL-c (32.3% vs. 47.7%; P = 0.034). The differences observed in other variables of interest were not significant. Combined dyslipidemia as athero-genic dyslipidemia in the whole group was seen in 15.5% and 69.1% of patients using conventional and international consensus criteria, respectively. In patients with abnormal albuminuria, these proportions were 16.1% and 65.6% using the same criteria, respectively; however, the differences between the two subgroups did not reach the level of statistical significance.


   Discussion Top


The results of the present post hoc analysis can be summarized as follows. First, abnormal albuminuria was present in half of T2DM patients with the majority having microalbu-minuria. Second, hypertension was more frequently seen in patients with abnormal albuminuria with most of them receiving RAS inhibitors. Third, abnormal albuminuria was associated with significantly lower cholesterol and non-HDL-c levels. Third, low HDL-c and elevated TG levels were patterns of isolated dyslipidemia more and less frequently seen in patients with abnormal albuminuria. Fourth, abnormal albuminuria was associated with atherogenic dyslipidemia as combined dyslipi-demia.

Abnormal albuminuria with mainly micro-albuminuria was present in half of T2DM patients in the present analysis. This finding is consistent with previous studies from[13],[25] and out-of-Africa[26] reporting that more than one-third of diabetic patients experience micro-vascular complications such as nephropathy. Metabolic abnormalities such as hyperglycemia, accumulation of advanced glycation end products, oxidative stress, and vasoactive renal factors including RAS and other vasoconstrictors have been reported to play a role in the development of diabetic nephropathy.[25],[26],[27]

Eighty patients with abnormal albuminuria had hypertension with most of them receiving RAS inhibitors. Hypertension is the most important risk factor for CVD and its prevalence increases in the presence of albumi-nuria.[28] Indeed, the prevalence of hypertension has been reported to range from 41% in participants with type 1 diabetes to 93% in those with type 2 diabetes and proteinuria.[28] Many studies have shown that angiotensin-converting enzyme inhibitors and angiotensin receptor blockers prevent or at least delay the development of microalbuminuria in patients with hypertension and type 2 diabetes, reduce the incidence of overt diabetic nephropathy, and are also beneficial in patients with non-diabetic renal disease. Therefore, RAS inhibittion plays a key role in the prevention of cardiovascular and renal outcomes.[28] As the majority of patients with hypertension will need at least two antihypertensive agents to achieve blood pressure goals, the use of RAS inhibitors is a mandatory part of antihyper-tensive therapy.[28]

Abnormal albuminuria was associated with lower cholesterol (TC and LDL-c) levels in the present post hoc analysis. In most studies on dyslipidemia in T2DM, levels of TC and LDL-c were within normal limits in patients with diabetic nephropathy.[29] However, a Chinese study found that macroalbuminuria was a risk factor for developing elevated TC and LDL-c levels.[30] In the present analysis, most T2DM patients had microalbuminuria than macro-albuminuria explaining possibly the observed TC and LDL-c levels. Lower levels of non-HDL-c, a well-known surrogate marker of Apo B-containing lipoproteins, were observed in T2DM patients with abnormal albuminuria. It has been reported that different types of dyslipidemia are associated with different stages of diabetic nephropathy.[30],[31],[32],[33],[34] In this regard, a progressive increase in TG levels with albuminuria, from normoalbuminuria to microalbuminuria and macroalbuminuria, has been already reported in T2DM.[11] Bearing this finding in mind, we can speculate that lower levels of non-HDL found in the present analysis could be explained in part by the fact that the majority of patients had micro-albuminuria rather than macroalbuminuria and mean TG levels within normal range.

Low HDL-c and elevated TG levels were patterns of isolated dyslipidemia most and less frequently seen in patients with abnormal albuminuria in the present analysis. Conflicting results have been reported about patterns of dyslipidemia in T2DM patients of African descent. If most studies such as ours reported low HDL-c levels and elevated TG levels as the most and less common patterns of dys-lipidemia in black T2DM patients,[5],[31],[32],[33] some studies, however, found elevated TG levels as the most common pattern of dyslipidemia.[34] Various patterns of dyslipidemia in T2DM patients could be due to varying sample size, variable duration of the disease, and BMI of the study samples.[35],[36]

Patients with abnormal albuminuria had an average TG level within normal range and lower frequency of elevated TG levels in the present analysis. This finding is consistent with data from previous studies reporting normal TG levels in overweight women of African descent[37] and does reflect the so-called “triglyceride paradox” reported in people of African descent.[38] This paradox relies upon the presence of hyperinsulinemia and the greater activity and less inhibition of lipoprotein lipase (LPL), enzymes that clear TG-rich lipoproteins from the circulation.[39]

Abnormal albuminuria was associated with atherogenic dyslipidemia in the present analysis. The association between atherogenic dyslipidemia and abnormal albuminuria has been reported to be bidirectional.[24],[34] The pathogenesis of atherogenic dyslipidemia in T2DM patients is complex, multifactorial; it relies mainly on the presence of insulin resistance and its negative impact on LPL and hepatic lipase activity, resulting in increased levels of free fatty acids delivered to the liver and subsequent overproduction of very-low-density lipoprotein-cholesterol (VLDL-c) leading to hypertriglyceridemia.[27],[36] Decreased LPL activity due to renal loss of apolipo-protein CII (apo CII) and increased apolipop-rotein CIII levels also contributes to accumulation of triglyceride-rich lipoproteins. Accumulated VLDL-c could stimulate the exchange of TG to cholesterol ester from HDL-c and LDL-c with a subsequent increase in catabolic rate of HDL-c and conversion of LDL-c to small and dense LDL-c particles.[27],[36] On the other hand, the loss of glomerular selectivity because of progression of diabetic nephropathy can promote HDL hypocholesterolemia.[36]

Atherogenic dyslipidemia can induce glome-rular injury and albuminuria through the activation of transforming growth factor-beta (TGFβ) pathway and subsequent generation of reactive oxygen species.[27],[36] The activation of TGFβ pathway also increases matrix deposition in the tubulointerstitium and mesangium. Triglyceride-rich lipoproteins can also activate monocytes and disrupt cellular glycocalyx, with subsequent increased permeability within the glomerulus. Oxidized lipoproteins can inhibit nitric oxide (NO)-mediated vasodilation, modulate mesangial proliferation, and increase monocyte chemoattractant expression, which all contribute to glomerular injury.[27],[36]

The interpretation of the results of the present analysis should take into account of some limitations. First, the post hoc analysis nature of the study precludes the establishment of temporal relationships between variables of interest. Second, the small sample does not confer much power to statistical tests to identify additional associations between variables of interest. Third, we did not measure co-factors of antioxidant enzymes to better explain the alterations in enzymes levels. Fourth, we did not evaluate insulin resistance, the pathogenic mechanism underlying the relationship between dyslipidemia and abnormal albuminuria in T2DM.


   Conclusion Top


Lipid profile in T2DM patients with abnormal albuminuria was characterized by lower cholesterol levels and a tendency toward elevated TG levels in comparison to those with normal albuminuria. Low HDL-c was the most common pattern of isolated dyslipidemia, and approximately 70% of patients with abnormal albuminuria had atherogenic dyslipidemia, a well-known cardiovascular and renal disease progression risk factor.

Conflict of interest: None declared.

 
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[PUBMED]  [Full text]  
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Correspondence Address:
Dr. Francois M Kajingulu
Department of Internal Medicine, Division of Nephrology, University of Kinshasa, Kinshasa
Democratic Republic of Congo
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1319-2442.235175

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