Cardiovascular comorbidity in рatients with end-stage renal disease: а рrospective single-center cohort study
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ISSN: 13412051
Volume 25, Issue 11, November, 2020
Cardiovascular comorbidity in рatients with end-stage
renal disease: а рrospective single-center cohort study
Iryna Shifris1, Iryna Dudar2, Еduard Krasiuk3
PhD of Medical Science, Leading Researcher of Efferent Technology Department, Institute of Nephrology
of the National Academy of Medical Sciences, Degtyarivska 17 V, 04050, Kyiv, Ukraine1
Professor of Nephrology, Head of Efferent Technology Department, Institute of Nephrology of the National
Academy of Medical Sciences, Degtyarivska 17 V, 04050, Kyiv, Ukraine2
PhD of Medical Science, Director of Municipal nonprofit enterprise «Kyiv Сity Сenter of Nephrology and
Dialysis», Petra Zaporozhets, 26, 02125, Kyiv, Ukraine3
ABSTRACT— The purpose of the study was to investigate the structure of cardiovascular comorbid states,
their frequency dynamic within the study period, as well as predictors of new-onsets events in end-stage
renal disease (ESRD) patients and its incidence rate depending on dialysis modality. The prospective
observational cohort study involved 326 ESRD patients, 223 of whom were treated with hemodialysis (HD)
and 103 with peritoneal dialysis (PD), between 2012 and 2019. Average duration of prospective observation
was 42.2 ± 26.4 months. Оf particular interest were new-onset cardiovascular diseases (CVD). Within the
observational timeframe the portion of CVD patients increased by 25.6% and 20.3%, when treated with HD
and PD respectively (p=0.2978). The incidence of coronary artery disease was significantly higher in HD
compared to PD patients. (23.8% to 8.8%, р = 0.0014; RR 2.7200; 95% СІ: 1.3961 – 5.2992). However, the
incidence of heart failure was higher in PD compared to HD patients (20.4% to 5.5%, р < 0.0001; RR
3.7888; 95% СІ: 1.9393 – 7.4023). The independent predictors of new-onset CVD in studied cohort were:
diabetes mellitus (HR 2.3116, 95% СІ: 1.5664 – 1.5664), history of MRSA carried (HR 2.1535, 95% СІ:
1.3578 – 3.4156), age (HR 1.0323, 95% СІ: 1.0183 – 1.0465), PD treatment (HR 1.8205, 95% СІ: 1.1259 –
2.9435), serum albumin levels (HR 0.9532, 95% СІ: 0.9122 – 0.9961). The observed results demonstrate an
over-time significant increase in frequency of CVDs in those suffering from ESRD. A difference was
established in the structure of new-onset CVD events, as well as their predictors, between PD and HD
groups.
KEYWORDS: end-stage renal disease, hemodialysis, peritoneal dialysis, cardiovascular disease,
comorbidity, predictor.
1. INTRODUCTION
The past three decades have been marked by significant prevalence of chronic non-communicable diseases.
In the list of Top 10 causes of death in the high-income countries for 2016 chronic kidney disease (CKD)
took 9th place [1], [2]. Cardiovascular diseases (CVD) remain the main cause of death in the general
population. The presence of CKD is known to be one of the leading accepted independent risk factors for
cardiovascular diseases. At the same time, CVD also remains the main cause of morbidity and mortality for
CKD patients. The CVD frequency increases along with the progression of CKD and reaches its maximum
when treated by renal replacement therapy (RRT) [1], [3]. According to the available studies, coronary
artery disease (CAD) and heart failure (HF) are the most common comorbid conditions. The prevalence of
coronary artery disease and heart failure at the start of renal replacement therapy, with significant
fluctuations in European countries, is 25% and 22.3%, respectively. Furthermore, a recently published
EURODOPPS study showed that the frequency of CAD and HF in a large cohort of hemodialysis (HD)
patients in the European countries amounted to 36.6% and 20.5%, respectively. Other CVDs were reported
3445I. Shifris, I. Dudar and Е. Krasiuk, 2020 International Medical Journal
in 33% of patients according to the same study [4], [5]. The frequency of CAD in end-stage renal disease
(ESRD) patients treated by hemodialysis and peritoneal dialysis (PD) for more than 90 days in the United
States is 42.3% and 34.4% respectively. Similarly, the frequency of HF is 40.4% and 28.3% for HD and
PD, respectively. The proportion of patients with acute myocardial infarction events is 14.0% among
hemodialysis patients and 11.6% among the peritoneal dialysis patients; atrial fibrillation is seen in 19.6%
and 14.1% of the patients, respectively. Overall, with significant fluctuations depending on age, CVDs are
present in more than 70% of HD patients and in 58% of PD patients among the US ESRD population. [6]
Research data shows that after the start of dialysis treatment the proportion of patients with CVD
significantly increases. In particular, CAD and HF prevalence increased by 10.2% and 13.6% respectively,
over the 2.2-year period. Overall, new-onset CVDs were registered in more than 10% of patients 2.2 years
after the HD initiation. The above deserves particular attention due to the significant increase in the
frequency of hospitalization and readmission of the dialysis population [7], [8], [9]. CVD mortality is 10-20
times higher among ESRD patients than in the general population. These comorbid conditions are
responsible for 40-50% deaths in patients treated by RRT dialysis methods. Regardless of the dialysis
modality, sudden cardiac death amounts to over 70% of events in the structure of CV mortality [10], [11],
[12].
Significant CVD frequency in ESRD patients is due to the high prevalence of both traditional
(hypertension, diabetes mellitus, dyslipidemia, smoking, advanced age) and non-traditional, the so-called
uremic, cardiovascular risk factors. The most significant among the latter are anemia, hyperphosphatemia,
hyperhydration, existing left ventricular hypertrophy, nutritional disorders, type of vascular access,
asymptomatic carriage of methicillin-resistant S. aureus (MRSA) and comorbid infectious diseases [13],
[14], [10], [15], [16], [17], [18]. The results of existing studies on the effect of dialysis modality on CVD
development risks remain inconsistent. In particular, cardiovascular risks were significantly higher in PD
patients compared with HD patients according to researchers from Saudi Arabia. Similar data was obtained
by researchers from Turkey. Meanwhile, the CAD risk in Taiwan's dialysis population did not significantly
differ regardless of the RRT modality. [19], [11], [20], [7]. There are other aspects associated with the
frequency and prognosis of CVD which have not been confirmed in the dialysis population. In particular,
there are ongoing discussions regarding the calcification of heart valves and coronary arteries, arterial
stiffness and rigidity, natriuretic peptides as risk factors for the development, and progression of CVD in
ESRD patients who are not on the kidney transplant waiting list [21], [7], 22]. As of today, serious negative
consequences of CVD for clinical results in ESRD patients are not in doubt. However, experts draw
attention to the limited number of available studies analyzing the frequency of both existing and newly
diagnosed CVDs, as well as risk factors for their occurrence depending on the RRT dialysis modality. They
emphasize the urgent need for in-depth research in an attempt to reduce comorbid condition prevalence,
including CVD, among the specified cohort of patients, and to more thoroughly study the factors enhancing
them [23], [24]. And finally, even the existing data from a small number of available studies regarding the
CVD frequency and structure, and risk factors of their development in ESRD patients most probably cannot
be extrapolated on a full scale to the dialysis population of Ukraine due to the differences in the patients’
nosological and age structure as well as racial characteristics.
1.1 The purpose
of the study was to investigate the structure of cardiovascular comorbid conditions, their frequency dynamic
during the study period, proportion and predictors of the new-onsets in ESRD patients taking into account
RRT modality.
2. Materials and methods
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2.1 Study Design and Subjects
The prospective observational longitudinal cohort study included 326 ESRD patients who were treated by
RRT dialysis methods during 2012-2019 in the Kyiv Municipal Scientific and Practical Center of
Nephrology and Dialysis, which is the clinical site of the Institute of Nephrology of the Academy of
Medical Sciences of Ukraine. The average duration of treatment by RRT methods at baseline was 26.5 ±
11.2 months. Each patient signed an informed consent form to participate in the study. The study protocol
was approved by the local ethics commission of the Institute of Nephrology of the Academy of Medical
Sciences of Ukraine. The research of the most common CVD in the study population was carried out on the
basis of clinical and laboratory examination as well as the results of instrumental studies and advisory
opinions of related specialists. The entry criteria for patients were as follows: age over 18, treatment by
RRT dialysis methods, ability to adequately cooperate in the research process. The exclusion criteria were
age under 18, total weekly Kt/VI. Shifris, I. Dudar and Е. Krasiuk, 2020 International Medical Journal
considered statistically significant. Factors contributing to the onset of heart disease events were examined
using multivariate Cox proportional hazards regression analysis. Cox proportional hazards model was
constructed for the study population, HD groups, and PD groups.
3. Results
The total number of 326 patients included 110 females (33.74%) and 216 males (66.26%). The patients' age
ranged from 20 to 85 years, with a mean age of 57.75 ± 14.58 years and the most common cause of ESRD
being glomerulonephritis (188 patients; 57.67%). Demographic and clinical data at baseline, categorized by
dialysis modality, are provided in Table 1.
Table 1. Baseline characteristics of the study population by dialysis modality
Patient groups
Parameter Group I Group II P
(HD patients, n =223) (PD patients, n =103)
Demographics and clinical characteristics
Age (years; М ±SD) 49.4±14.03 55.6±14.72 0.0003
Male (n/%) 151/67,7 65/63,1 0.4150
Body mass index (kg/m²; М ±SD) 24.29±4.32 25.14±4.74 0.1100
Dialysis duration (months; М ±SD) 27.3±11.22 4.04±2.93ISSN: 13412051
Volume 25, Issue 11, November, 2020
parathyroid hormone; MRSA, methicillin-resistant staphylococcus aureus; NA, not applicable; Me, median;
IR, interquartile range[Q25-Q75]. The duration of RRT treatment was significantly higher in HD patients
when compared to PD patients, and lasted 27.3 ± 11.22 and 4.04 ± 2.93 months respectively (pI. Shifris, I. Dudar and Е. Krasiuk, 2020 International Medical Journal 2.7200; 95% SI: 1.3961 – 5.2992; p=0.0033) times higher than in the PD group. At the same time, the PD group had a higher risk of HF in comparison with the HD group (RR 3.7888; 95% SI: 1.9393 – 7.4023; p=0.0001). PD treatment also led to a significantly higher frequency of new HF events than HD treatment (χ²=17.163, p
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loss of communication (n=17) and renal transplantation (n=14). A total of 125 patients (38.3%) died during
the study period. The incidence rates of all-cause mortality were 15.14 per 100 patient-years. The leading
causes of mortality were cardiac events, accounting for 52% of all deaths (7.85 per 100 patient-years).
Infectious processes were responsible for 24.8 % of deaths, mortality rate was 3.75 per 100 patient-years.
Table 4. Outcomes in study population by treatment modality
Parameter Group I Group II P
(HD patients, n =223) (PD patients, n =103)
n/% incidence n/% incidence
rate rate
Follow-up duration 579.3 249.2 0.000037
(patient-years)
Renal 10/4.48 1.73 4/3.88 1.61 0.8040
transplantation
Lost to 12/5.38 2.07 5/4.85 2.01 0.8416
communication
Cause of death
Cardiac disease 43/19.28 7.43 22/21.34 8.82 0.6656
Infectious disease 19/8.52 3.28 12/11.65 4.8 0.3712
Cerebrovascular 9/4.04 1.55 5/4.85 2.01 0.7378
disease
Other 10/4.48 1.73 5/4.85 2.01 0.8823
Total deaths 81/36.3 13.98 44/42.7 17.7 0.2699
Abbreviations: HD, Hemodialysis; PD, Peritoneal Dialysis; Incidence rate are expressed as per 100 patient-
years
4. Discussion
There have been significant advances in the field of dialysis technology in the last three decades, however,
the high morbidity and mortality of ESRD patients still remains one of the most severe problems of modern
nephrological practice. As of today, it is well-known that CVD is the leading cause of morbidity,
hospitalization and mortality in the dialysis population [7], [8], [9], [26], [10], [11]. On the topic of the
prevalence of certain CVDs, it should be emphasized that most of the available studies are conducted as a
cross-sectional study; that is, they are limited because data is only collected once, at a specific point in time,
meaning it doesn't reflect the parameter dynamic. Longitudinal studies that demonstrate changes in the
prevalence of CVD among the ESRD population, over a period of time, are rather limited. Meanwhile,
similar studies investigating the PD population are absent altogether. The most significant contribution of
present research is the study of incidence and medium-term dynamic of both CVD in general as well as
separate nosological forms. As far as we are aware, the current study has no analogues, being the first
comprehensive longitudinal analysis of the prevalence of cardiovascular comorbidity, the dynamic of
changes in its frequency, the significance of predictors of new events in ESRD patients, and all-cause
mortality depending on RRT dialysis modality. Most available studies analyze the prevalence of the most
common comorbid CVDs including CAD and HF in the ESRD population. The CAD frequency varies
depending on the RRT modality and, in the dialysis population of the United States, amounts to 42.3% and
34.4% with HD and PD treatment, respectively [6]. On the other hand, the CAD frequency in the HD
3451I. Shifris, I. Dudar and Е. Krasiuk, 2020 International Medical Journal
population of Europe is 36.6% according to [5]. The data obtained in the course of the current study comes
close to confirming the results received by researchers from the United States and Europe. In particular, at
baseline, in the studied cohort, CAD was registered in 23.3% of the HD patients and 22.3% of the PD
patients. The results of research studies on HF prevalence indicate that the condition is present in more than
40% of HD and 28% of PD patients in the United States [6]. The results of the current study present
somewhat different data. At baseline, HF was registered in 14.7% and 18.4% of HD and PD patients,
respectively. Meanwhile, the indicator dynamics analysis showed that the HF frequency more than doubled
in patients undergoing PD treatment (18.4% vs 38.8%) during the observation period and grew only by
37.4% in HD patients. At the same time, the incidence dynamics analysis of CAD shows its significant
increase during the observation period in HD patients compared to PD patients (47.1% vs 31.1%). During
the follow-up, 62 CAD events were registered in the studied cohort for the first time with the overwhelming
majority being in the HD group (53 events; p=0.0033). The number of HD patients with CAD doubled
during the same period (23.3% vs 47.1%). Similar data regarding the increase in the number of CAD and
HF patients over a mean of 2.2 years of treatment by RRT dialysis were published by [7]. However, the
results of the mentioned study only show the proportion of new-onset CVD events that occurred after the
start of RRT treatment in ESRD patients without a history of CV pathology. The data on the increase of the
CVD frequency in HD patients over time have also been reported by researchers in Canada. But the results
of their study were based solely on the registration of CVD cases that caused hospital readmission and/or
the patient's death [8]. The prevalence analysis of other CVDs (atrial fibrillation, AMI and other heart
diseases) allowed us to confirm that the data we received correspond with the results obtained by
researchers from the USA [6].
It is well-known that the frequency of CVD events in PD patients is associated with a significant prevalence
of both traditional and non-traditional (including dialysis-associated) cardiovascular risk factors [13], [14],
[26], [15], [16], [17], [18]. According to the study by anemia, serum calcium and phosphorus levels were
independent risk factors for CVD in HD patients [10]. I-Kuan Wang et al. found no difference in the overall
risk of de novo CAD events between HD and PD. At the same time, HD was associated with a higher risk
of de novo HF compared to PD in patients' first year after starting dialysis [20]. In a recently published
study, demonstrated that PD treatment and age were significant predictors of emergency hospitalization and
mortality for CVDs in Cox proportional hazards regression model for the dialysis population of Japan [27].
Sharabas I et al. stated that Saudi patients undergoing PD have worse CVD risk profiles compared to HD
patients. Meanwhile, in the Cox proportional hazard regression model for CV events age greater than 57
years, and the use of more than 1 type of antihypertensive medication were associated with increased risk,
while EF over 53 was associated with reduced risk [19]. According to Harmankaya O et al., cardiovascular
risk factors were more frequent in PD rather than HD patients [11]. We did not analyze the risk factors for
CVD mortality. Nevertheless, based on the results of our research we support the data presented by the
scientists from Japan, Saudi Arabia and Turkey [27], [19], [11]. Our data let us conclude that significant
predictors of all new-onset CVD events in the Cox proportional hazard regression model for the studied
cohort were age, PD, history of MRSA carried, serum albumin level, and diabetes mellitus as the primary
cause of ESRD. However, initial vascular access, history of MRSA carried, age, and serum albumin levels
were significant independent predictors of all new-onset cardiovascular events in the HD group. The history
of MRSA carried, overhydration, diabetes mellitus, and age level were significant independent predictors of
all new-onset cardiovascular events in the PD group. The present study confirmed the data produced by
numerous studies on CVD that claim it is the leading cause of all-cause mortality [5], [6], [11], [17], [18],
[24], [27]. That being said, the current study has certain limitations being just a single-center study. The
results should be further confirmed by multicenter studies with a large sample size and a single protocol. In
addition, this study did not separately identify risk factors for the most common new-onset CVD events,
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namely CAD and HF. At the same time, the results of a medium-term prospective observational cohort
study, conducted on sufficient clinical material, allowed us, for the first time, to determine the frequency, as
well as independent predictors and risks of developing new-onset CVDs both for the studied cohort overall,
and depending on the RRT dialysis modality.
5. Conclusions
In conclusion, our study demonstrated a high prevalence of cardiovascular diseases with both HD and PD
treatment. The frequency of all new-onset CVD events during the study period did not differ much between
the compared groups. However, we observed that the CVD frequency at the end of study, as well as the risk
of new CAD events were significantly higher in the HD group. At the same time, similar indicators for HF
were significantly higher in the PD group. The independent predictors of all new-onset cardiovascular
events for the studied cohort were age, PD treatment, history of MRSA carried, diabetes mellitus as the
primary cause of ESRD, and serum albumin levels.
6. References
[1] orld Health rganization. (2006). Stop the global epidemic of chronic disease: a practical guide to
successful advocacy. World Health Organization. https://apps.who.int/iris/handle/10665/43513
[2] Global Health Estimates 2016: Deaths by Cause, Age, Sex, by Country and by Region, 2000- 2016.
(2018) Geneva, Switzerland: World Health Organization;
http://www.who.int/healthinfo/global_burden_disease/estimates/en/. Accessed November 16, 2018.
[3] CKD and Coronary Artery Disease: A KDIGO Conference Report/ Sarnak et al. J Am Coll Cardiol.
2019;74(14):1823– 38. DOI: 10.1016/j.jacc.2019.08.1017.
[4] Changes in co-morbidity pattern in patients starting renal replacement therapy in Europe—data
from the ERA-EDTA Registry. / Ceretta M. L. et al. / Nephrology Dialysis Transplantation. 2018. Vol. 33:
1794–1804. DOI: https://doi.org/10.1093/ndt/gfx355.
5 Liabeuf S, Sajjad А, Kramer А, Bieber В, McCullough К, Pisoni R, et al. (2019). Guideline attainment
and morbidity/mortality rates in a large cohort of European haemodialysis patients (EURODOPPS). /
Nephrology Dialysis Transplantation, 34 (12), pp. 2105–2110. https://doi.org/10.1093/ndt/gfz049.
[6] United States Renal Data System. (2018) USRDS annual data report: Epidemiology of kidney
disease in the United States. National Institutes of Health, National Institute of Diabetes and Digestive and
Kidney Diseases. Available at: https://www.usrds.org/2018/view/Default.aspx.
[7] Bansal N. (2017). Evolution of Cardiovascular Disease During the Transition to End-Stage Renal
Disease. Seminars in Nephrology, 37(2), pp..120-131. DOI: 10.1016/j.semnephrol.2016.12.002.
[8] Harel Z, Wald R, McArthur E, Chertow, G., Harel, S., Gruneir, A., et al. (2015). Rehospitalizations
and Emergency Department Visits after Hospital Discharge in Patients Receiving Maintenance
Hemodialysis. J Am Soc Nephrol, 26(12), pp. 3141–3150. doi: 10.1681/ASN.2014060614/
[9] Erickson KF, Winkelmayer WC, Chertow GM, Bhattacharya J. (2014). Physician visits and 30-day
hospital readmissions in patients receiving hemodialysis. J Am Soc Nephrol, 2014, 25(9), pp. 2079-2087.
doi: 10.1681/ASN.2013080879.
3453I. Shifris, I. Dudar and Е. Krasiuk, 2020 International Medical Journal
[10] Panjiyar R, Sharma R, Laudari S, Gutpa M, Ghimire M, Subedi P, Subramanyam G. (2017).
Cardiovascular complications in end stage renal disease in a tertiary hospital in Nepal. JCMS Nepal, 13 (2),
pp. 279-83.
[11] Harmankaya O, Akalin N, Akay H, Okuturlar Y, Erturk K, Kaptanogullari H, et al. (2015).
Comparison of risk factors for cardiovascular disease in hemodialysis and peritoneal dialysis patients.
Clinics, 70(9), pp..601-605.
[12] Genovesi S, Boriani G, Covic А, Vernooij R, Combe С , Burlacu А, et al. (2019). Sudden cardiac
death in dialysis patients: different causes and management strategies. Nephrol Dial Transplant. 2019; 1–10.
doi: 10.1093/ndt/gfz18. Available at: https://academic.oup.com/ndt/advance-article-
abstract/doi/10.1093/ndt/gfz182/5571895 by guest on 01 May 2020.
[13] Cozzolino М, Mangano М, Stucchi А, Ciceri Р, Conte F, Galassi А. (2018). Cardiovascular disease
in dialysis patients. Nephrol Dial Transplant, 33, iii28–iii34. doi: 10.1093/ndt/gfy174.
[14] Shifris I.M. (2020). Diabetic status, comorbidity and survival in patients with chronic kidney
disease stage VD st.: a cohort study. Problems of endocrine pathology. 2020; 2, pp.. 95-103,
https://doi.org/10.21856/j-pep.2020.2.12
15 Shifris І, Dudar I, Gonchar I , Krasyuk E., Prusskiy F, & Вurhynska I. (2016). Vascular access options
at hemodialysis therapy initiation: complications and survival of patients with chronic kidney diseas stage 5
D. Ukrainian Journal of Nephrology and Dialysis. 3(51); 37–41.
https://doi.org/10.31450/ukrjnd.3(51).2016.05.
[16] Malik J. (2018). Heart disease in chronic kidney disease – review of the mechanisms and the role of
dialysis access. The Journal of Vascular Access, 19(1), pp..3-11. https://doi.org/10.5301/jva.5000815.
17 Vervloet M, Sezer S, Massy Z, Johansson L, Cozzolino М, Fouque D. (2017). The role of phosphate in
kidney disease. Nat Rev Nephrol, 13, pp. 27–38. doi:10.1038/nrneph.2016.164.
18 Shifris І, Dudar I, Krot V, Kruglikov V, Aleksieva N, Nechyporuk T, et al. (2015) Аntimicrobial
resistance of gram positive bacteria isolated in patients with chronic kidney diseas stage 5 D: prevalence
and outcomes. Ukrainian Journal of Nephrology and Dialysis, 2015; 2(46): 13-21. doi:
https://doi.org/10.31450/ukrjnd.2(46).2015.02.
[19] Sharabas I, Siddiqi N. (2016). Cardiovascular disease risk profiles comparison among dialysis
patients. Saudi J Kidney Dis Transpl, 27, pp. 692-700. doi: 10.4103/1319-2442.185225.
[20] Wang IK, Lu CY, Lin CL, Liang CC, Yen TH, Liu YL, et al. (2016) Comparison of the risk of de
novo cardiovascular disease between hemodialysis and peritoneal dialysis in patients with end-stage renal
disease. Int J Cardiol., 218, pp. 219– 224. doi: 10.1016/j.ijcard.2016.05.036.
[21] Tian Y, Feng S, Zhan Z, Lu Y, Wang Y, Jiang S, et al. (2016). Risk Factors for New-Onset Cardiac
Valve Calcification in Patients on Maintenance Peritoneal Dialysis. Cardiorenal medicine, 6(2): pp. 150–
158. https://doi.org/10.1159/000443620.
3454ISSN: 13412051
Volume 25, Issue 11, November, 2020
[22] Segall L, Nistor I, Covic A. (2014) Heart Failure in Patients with Chronic Kidney Disease: A
Systematic Integrative Review. BioMed Research International, Article ID 937398, 21 pages. [online].
Available at: http://dx.doi.org/10.1155/2014/937398.
[23] Kovesdy CP. (2019). Clinical trials in end-stage renal disease-priorities and challenges. Nephrol
Dial Transplant, 34(7), pp. 1084‐1089. doi:10.1093/ndt/gfz088.
[24] Jager KJ, Lindholm B, Goldsmith D et al. (2011). Cardiovascular and non-cardiovascular mortality
in dialysis patients: where is the link? Kidney Int Sup, 1, pp..21-23. doi: 10.1038/kisup.2011.7.
[25] Al-Fartosy AJM, Awad NA, Mohammed AH. (2020) Intelectin-1 and Endocrinological Parameters
in Women with Polycystic Ovary Syndrome: Effect of Insulin Resistance. Ewha Med J., 43(1), pp. 1-11.
[26] Stepanova N, Burdeyna O. (2019). Association between Dyslipidemia and Peritoneal Dialysis
Technique Survival. Open Access Maced J Med Sci. 2019 Jul 25;7(15):2467-2473. doi:
10.3889/oamjms.2019.664. PMID: 31666849; PMCID: PMC6814482.
[27] Banshodani, M., Kawanishi, H., Moriishi, M., Shintaku, S., & Tsuchiya, S. (2020). Association
between Dialysis Modality and Cardiovascular Diseases: A Comparison between Peritoneal Dialysis and
Hemodialysis. Blood Purification, 49, pp.302–309.
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