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CORRELATION OF CARDIOVASCULAR RISK WITH RENAL DYSFUNCTION
FACTORS IN STABLE ANGINA
Rakhimova M.E.
Gadaev A.G.
Tashkent Medical Academy No. 2 Department of Internal Medicine in Family Medicine.
Tashkent, Uzbekistan.
https://doi.org/10.5281/zenodo.15063714
Abstract. Ischemic heart disease is one of the main causes of disability and death among
the population all over the world, including in Uzbekistan. Among the comorbid conditions
observed in this group of patients, kidney dysfunction is of particular importance, and even the
earliest subclinical disorder affects the exacerbation of the main disease and the development of
complications, as well as mortality rates as an independent risk factor. This article aims to
investigate the significance of creatinine, cystatin C, proteinuria and podocyturia in early
diagnosis of RD in patients with stable angina pectoris and their association with cardiovascular
risk. Cystatin C has been reported to be reliably effective compared to serum creatinine in the
early diagnosis of RD in patients with stable angina pectoris. It has also been confirmed that
podocyturia is one of the main markers for its early detection and assessment of its progression.
Key words: ischemic heart disease, risk factor, dyslipidemia, renal dysfunction,
glomerular filtration rate, cystatin S, creatinine, podocyturia.
КОРРЕЛЯЦИЯ СЕРДЕЧНО-СОСУДИСТОГО РИСКА С ФАКТОРАМИ
НАРУШЕНИЯ ФУНКЦИИ ПОЧЕК ПРИ СТАБИЛЬНОЙ СТЕНОКАРДИИ
Аннотация. Ишемическая болезнь сердца является одной из основных причин
инвалидизации и смертности населения во всем мире, в том числе и в Узбекистане.
Среди сопутствующих заболеваний, наблюдаемых у данной группы больных, особое
значение имеет нарушение функции почек, причем даже наиболее раннее субклиническое
нарушение влияет на обострение основного заболевания и развитие осложнений, а также
на показатели смертности как независимый фактор риска. Целью данной статьи
является исследование значения креатинина, цистатина С, протеинурии и подоцитурии в
ранней диагностике РЗ у больных стабильной стенокардией и их связи с сердечно-
сосудистым риском. Сообщается, что цистатин С достоверно эффективен по сравнению
с сывороточным креатинином в ранней диагностике РЗ у больных стабильной
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стенокардией. Также подтверждено, что подоцитурия является одним из основных
маркеров для ее раннего выявления и оценки ее прогрессирования.
Ключевые слова: ишемическая болезнь сердца, фактор риска, дислипидемия,
нарушение функции почек, скорость клубочковой фильтрации, цистатин S, креатинин,
подоцитурия.
Among the comorbid conditions observed in patients with ischemic heart disease (IHD),
renal dysfunction (RD) is of particular importance and is included in the group of leading risk
factors (RF) aggravating cardiovascular system diseases (CSD). [4,7]. Epidemiological and
population studies show that even the earliest subclinical impairment of kidney function affects
the development of CKD and its complications and mortality as an independent risk factor. When
kidney function impairment (KFI) occurs alongside conventional cardiovascular diseases (CVD),
it leads to slow-progressing inflammation, endothelial dysfunction, and activation of the
sympathoadrenal system (SAS). This also results in damage to atherosclerotic plaques (erosion,
calcification). [4, 5, 7, 10, 13, 16] The activation of the SAS further increases the risk of developing
acute coronary syndrome (ACS) and worsens the consequences of KFI. [9, 12] Coronary
angiography studies showed a 28% rate of three-vessel coronary artery disease (stenosis exceeding
50%) in patients with normal or slightly impaired kidney function, while this figure rose to 53%
in patients with moderate to severe KFI. [7, 10, 14, 16] Pathological processes in the kidneys are
traditionally assessed based on serum creatinine levels, estimated glomerular filtration rate
(eGFR), and micro- and macroalbuminuria (MAU). MAU development signifies sclerosis of 20-
25% of nephrons, and its progression to proteinuria indicates the loss of 50-70% of glomeruli. [1,
9, 12, 14, 15, 21] Studies have proven that albuminuria levels of 30-300 mg/day, or even 10-30
mg/day, significantly increase the risk of developing ACS and overall mortality. [5, 16, 18, 21]
According to research by Kotseva K., Saritas T., Floege J., and Belyalov F.I., the presence of
persistent proteinuria in patients with CVD, diabetes mellitus (DM), and hypertension (HT)
indicates damage to 70-80% of nephrons and the development of chronic kidney disease (CKD).
[2, 3, 4, 16, 22] Recent studies have utilized cystatin C as a biological marker for predicting CKD
development in patients with CVD. [5, 13, 14] Cystatin C levels in serum are more stable than
creatinine and less affected by factors like age, gender, muscle mass, and dehydration. Its clinical
sensitivity and specificity for kidney damage are reported as 86% and 82%, respectively. [6, 15,
18].
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The role of podocytes and podocyte-associated molecules in glomerular filtration and the
development of proteinuria is gaining significance. Podocytes, crucial components of the
glomerular structure, maintain the integrity of the filtration barrier and participate in other
important processes. [3, 17, 19, 20, 22] Detecting podocytes in urine has emerged as a valuable
tool for early diagnosis of pathological changes, surpassing the sensitivity of traditional
examinations. [8, 19, 20] Considering these findings, our research aims to investigate the
correlation between creatinine, cystatin C, proteinuria, and podocyte dysfunction in patients with
stable angina pectoris, along with their association with cardiovascular risk factors, for the purpose
of early diagnosis of KFI.
Material and methods:
This study included 167 patients with stable angina pectoris (II-
III-IV functional class) aged 61.47±8.42 years who were treated at the cardiology and cardiac
rehabilitation departments of the multidisciplinary clinic of Tashkent Medical Academy from 2020
to 2022. A control group of 36 volunteers (average age 62.4±8.5, 22 males and 14 females),
matched for age and gender, who did not have ACS, was selected for comparison.
The main group consisted of 112 (67.1%) males (average age 61.29±8.3) and 55 (32.9%)
females (average age 61.85±8.7). The diagnosis was based on the classification criteria adopted
by the European Society of Cardiology [12]. Initially, all patients underwent assessment of their
complaints, medical history, clinical condition during objective examination, quality of life,
general urinalysis, complete blood count, biochemical and coagulation system blood tests, lipid
spectrum, serum creatinine and cystatin C levels, as well as proteinuria and podocyturia in urine.
All patients underwent ECG, 24-hour Holter monitoring (based on indications),
echocardiography, and renal artery Doppler ultrasound (if necessary). In addition, the GFR was
calculated based on serum creatinine and cystatin C levels, and the obtained results were analyzed
comparatively.
Results: Based on the obtained results, all patients in the main group were divided into two
subgroups. The first subgroup consisted of 111 patients with preserved kidney function, and the
second subgroup consisted of 56 patients with existing KFI, with average ages of 58.6±0.71 and
61.2±0.97 years, respectively.
The patients in these subgroups were analyzed comparatively based on age, gender,
comorbidities, and existing CVD (Table 1).
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Table 1
Correlation of risk factors in ischemic heart disease with markers of renal dysfunction
Indicators
All patients, n=167
eGFR ≥ 90
ml/minute/1,73 м
2
(n=111)
eGFR ≤89
ml/minute/1,73 м
2
(n=56 та)
p
Number of men
91 (81,9%)
21 (37,5%)
X
2
=33.34
P<0.001
Number of women
20 (18.1%)
35 (62,5%)
X
2
=33.34
P<0.001
Average age
58,6±0,71
67,16±0,97
P<0.05
Number of diabetes
17 (15.3%)
20 (35,7%)
X
2
=8.98
P<0.001
Number of smokers
22 (19.8%)
8 (14,3%)
X
2
=0.774
P>0.05
Arterial hypertension, number
91 (82%)
50 (89,3%)
X
2
=33.34
P<0.001
The number of people who had a
myocardial infarction
27 (24,3%)
20 (35,7%)
X
2
=36.41
р<0,001
Number of anemia
26 (23,4%)
23 (41,1)%
X
2
=18.29
(р<0,001)
Number of people with a history of
stroke, %
12 (10,8%)
8 (13,8%)
X
2
=0.038
P>0.05
Proteinuria, number, %
31 (28,8%)
43 (76,8%)
P<0.05
According to the data presented in Table 1, men comprised 81.9% of the first group and
37.5% of the second group (X2=33.34 P<0.001). Women, on the other hand, were more prevalent
in the second group compared to the first, at 18.1% and 62.5%, respectively (X2=33.34 p<0.001).
Notably, the second group consisted of significantly older patients (p<0.005). When analyzing
the prevalence of comorbidities in the two groups, the following findings emerged: DM was
present in 15.3% /35.7% (X2=8.98 P<0.001), HT in 82.0% /89.3% (X2=33.34, p<0.001), anemia
in 23.4% /41.1% (X2=18.29 p<0.001), history of myocardial infarction (MI) in 24.3% /35.7%
(X2=36.41, p<0.001), stroke in 10.8 /13.8% (X2=0.038 p>0.05), and the comorbidity index (CI)
was 7.3 /8.7 points (p<0.001). Proteinuria was detected in 28.8% of patients in the first group and
76.8% of patients in the second group (p<0.05).
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The majority of indicators were significantly higher in the second group. Arterial blood
pressure was 141.4±1.8/85.5±1.7 mm Hg in the first group and 148.9±2.8/92.4±1.9 mm Hg in
the second group (p˂ 0.05/ P˂ 0.01). Blood glucose levels were 5.7±0.09 mmol/L in the first
group and 6.3±0.1 mmol/L in the second group (p<0.05), while hemoglobin levels were
114.6±1.3/107.8±1.5 g/L (p<0.001). Analysis of lipid profiles revealed the following in both
groups: total cholesterol (TC) - 6.2±0.04/6.8±0.05 mg/dL (p˂0.001), triglycerides (TG) -
3.0±0.01/ 3.4±0.02 mg/dL (p˂0.001), low-density lipoprotein cholesterol (LDL-C) - 4.7±0.03/
5.1±0.02 mg/dL (p˂0.001), very low-density lipoprotein cholesterol (VLDL-C) -
0.8±0.01/1.0±0.01 mg/dL (p˂0.001), and atherogenic index (AI) - 4.5±0.02/5.1±0.03 (p˂0.001).
These indicators were significantly higher in patients with existing KFI (p˂0.001). While HDL-
C was low in both groups, it did not differ significantly between the second (1.3±0.02) and the
first (1.4±0.01) groups. The higher levels of lipid profile changes, proteinuria, serum creatinine,
and anemia observed in patients in the second group suggest a strong association with their
existing KFI. Serum creatinine levels were 65.8±0.6 mmol/L in the first group and 73.14±1.0
mmol/L in the second group, while cystatin C levels were 1.2±0.01 mg/L and 1.3±0.02 mg/L,
respectively (p<0.001, p< 0.05). GFR calculations based on serum creatinine showed a value of
99.9±1.6 mL/min/1.73 m² in the first group and 79.9±1.4 mL/min/1.73 m² in the second group
(P<0.001). When GFR was calculated based on cystatin C in all patients, it was 91.8±1.6
mL/min/1.73 m² and 72.4±1.3 mL/min/1.73 m², respectively, showing a significantly lower value
compared to calculations based on creatinine (p<0.001) (Table 2).
Table 2
Comparative analysis of indicators of renal functional status determined by creatinine and
cystatin C in cross-sectional groups.
Indicators
eGFR ≥ 90
ml/minute/1,73 м
2
n=111(66,5%)
eGFR ≤89
ml/minute/1,73 м
2
n=56 (33,5%)
P
Creatinine, (mmol/l)
65,8±0,6
73,14±1,0
P<0.001
Cystatin S, (mg∕l)
1,2±0,01
1,3±0,02
P<0,05
xKFT based on creatinine,
ml/min/1.73m2
99,9±1,6
79,9±1,4
P<0.001
xKFT based on cystatin C,
ml/min/1.73m2
91,8±1,6
72,4±1,3
P<0.001
Proteinuria, (g/l)
0,005±0,018
0,017±0,048
P>0,05
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Among all patients in the control group, those with GFR ≥ 90 ml/min/1.73 m² constituted
59.3%, while those with GFR ≤ 89 ml/min/1.73 m² accounted for 40.7% (p<0.05). Based on these
results, 7.2% more cases of KFI were identified when GFR was calculated using cystatin C
compared to creatinine-based calculations (p<0.05).
Although no specific signs of KFI were observed based on patient complaints, medical
history, and clinical and laboratory test results, renal dysfunction was detected in 33.5% / 40.7%
of patients when GFR was calculated based on serum creatinine and cystatin C, respectively. When
comparing proteinuria between the groups, although the second group showed a 29.4% increase
compared to the first group, the result was not statistically significant.
The correlation between KFI and cardiac hemodynamic parameters was analyzed. Based
on these results, a very weak positive correlation was observed between creatinine and end-
diastolic dimension (EDD) (r=0.23, p˃0.05) and interventricular septum thickness (IVST) (r=0.2,
p˃0.05), while a very weak negative correlation was found with end-systolic dimension (ESD)
(r=-0.21, p˃0.05).
The correlation between these indicators and cystatin C was as follows: ejection fraction
(EF) (r=-0.25, p˃0.05) very weak, end-systolic volume (ESV) (r=-0.36, p<0.05) weak, ESD (r=-
0.51, p˃0.05) moderate inverse, EDD (r=0.4, p<0.01) and EDV (r=0.52, p<0.01) moderate
positive.
Based on these findings, cystatin C showed a higher correlation with cardiac hemodynamic
parameters compared to creatinine, indicating the possibility of evaluating systolic and diastolic
heart function based on cystatin C.
In patients in the first group, a very weak inverse correlation was observed between GFR
and ESD (r=-0.29, p˃0.05), and weak inverse correlations were found with EDD (r=-0.32, p<0.05)
and left ventricular posterior wall thickness (LVPT) (r=-0.31, p<0.05).
In the second group, a decrease in GFR showed a weak inverse correlation with EF (r=-
0.45, p<0.05), a moderate inverse correlation with ESV (r=-0.66, p<0.01), a strong inverse
correlation with ESD (r=-0.88, p<0.001), a weak correlation with LVPT (r=0.36, p<0.05), a
moderate correlation with EDD (r=0.53, p<0.01), and a strong positive correlation with end-
diastolic volume (EDV) (r=0.75, p<0.05) (Figure 1).
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Picture 1. Cardiorenal correlates in patients with stable angina pectoris
Note: IVST - interventricular septum thickness, LVPT - left ventricular posterior wall
thickness, EDV - end-diastolic volume, ESV - end-systolic volume, EDD - end-diastolic dimension;
ESD - end-systolic dimension, EF - ejection fraction, LV - left ventricle, LVMI - left ventricular
myocardial mass index.
Podocytes were not detected in the urine analysis of the control group. Podocyturia (PCU) (6.5-
11.2 ng/ml) was found in 73 (43.7%) patients in the main group.
When examined between the groups, PCU was found in 17 (15.3%) patients with GFR ≥ 90
ml/min/1.73 m² and in all (56 - 100%) patients with GFR ≤ 89 ml/min/1.73 m². At the same time, PCU
was 4.7 ± 0.06 ng/ml in the first group and 6.4 ± 0.08 ng/ml in the second group (P < 0.001).
Based on this result, PCU was significantly higher in patients with low GFR (P < 0.001). This
suggests that changes in the basement membrane of nephrons have occurred in patients with stable
angina pectoris, even in the absence of clinical and laboratory signs of KFI.
The correlation of PCU with KFI markers and other cardiovascular diseases (CVD) was
analyzed (Figure 2).
In patients in the first group, PCU showed a weak positive correlation with cystatin C (r=0.49,
p<0.05), total cholesterol (r=0.36, p<0.05), TG (r=0.33, p<0.05), low-density lipoprotein (LDL) and
very low-density lipoprotein (VLDL) (r=0.41, p<0.05), (r=0.46, p<0.05), respectively, and a moderate
positive correlation with the atherogenic coefficient (AC) (r=0.57, p<0.01).
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Picture 2. Correlation between podacituria, lipid spectrum and indicators of renal
function
Notes: GFR-Glomerular Filtration Rate, TG-Triglycerides, HDL-High-Density
Lipoprotein, VLDL-Very Low-Density Lipoprotein, LDL-Low-Density Lipoprotein, AC-
Atherogenic Coefficient
When this analysis was conducted on the second group of patients, a moderate positive
correlation (r=0.61, p<0.01) was observed between podocyturia (PCU) and cystatin C. A strong
negative correlation (r=-0.77, p<0.05) was found between PCU and GFR. These findings indicate
a statistically significant stronger relationship between markers of kidney function impairment in
the second group compared to the first group. The correlation between PCU and lipid parameters
did not differ from the results obtained in the first group. These results suggest that cystatin C and
PCU are important for the early detection of changes in kidney function in patients with stable
angina pectoris. Current tests are limited to detecting kidney damage (KD) in patients with stable
angina pectoris only at the stage of clinically significant albuminuria. However, KD often develops
earlier, even before microalbuminuria is detected. Our research showed that 15.3% of patients with
stable angina pectoris and GFR ≥ 90 ml/min/1.73 m², and 100% of those with GFR ≤ 89
ml/min/1.73 m² had podocyturia. Notably, none of the patients in the first group exhibited clinical
signs of KD. The presence of podocytes in urine in this context indicates the development of KD
and irreversible changes in the basement membrane of nephrons. Conclusion: Elevated cystatin C
levels and the associated decrease in GFR are more reliable indicators of KD than creatinine levels.
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When GFR is calculated based on cystatin C, the proportion of patients with KD increases
by 7.2% in the control group. This study confirms that the measurement of cystatin C levels and
the resulting GFR calculation are more reliable than creatinine levels and microalbuminuria for
the early detection of KD in this patient population. This early detection, along with the assessment
of the severity of the underlying disease and the risk of complications, allows for the prevention
of life-threatening complications, the selection of appropriate treatment strategies, and the
evaluation of their effectiveness.
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